Auditory corticocortical interconnections in the cat: evidence for parallel and hierarchical arrangement of the auditory cortical areas

Summary The origin and laminar arrangement of the homolateral and callosal projections to the anterior (AAF), primary (AI), posterior (PAF) and secondary (AII) auditory cortical areas were studied in the cat by means of electrophysiological recording and WGA-HRP tracing techniques. The transcallosal projections to AAF, AI, PAF and AII were principally homotypic since the major source of input was their corresponding area in the contralateral cortex. Heterotypic transcallosal projections to AAF and AI were seen, originating from the contralateral AI and AAF, respectively. PAF received heterotypic commissural projections from the opposite ventroposterior auditory cortical field (VPAF). Heterotypic callosal inputs to AII were rare, originating from AAF and AI. The neurons of origin of the transcallosal connections were located mainly in layers II and III (70–92%), and less frequently in deep layers (V and VI, 8–30%). Single unit recordings provided evidence that both homotypic and heterotypic transcallosal projections connect corresponding frequency regions of the two hemispheres. The regional distribution of the anterogradely labeled terminals indicated that the homotypic and heterotypic auditory transcallosal projections are reciprocal. The present data suggest that the transcallosal auditory interconnections are segregated in 3 major parallel components (AAF-AI, PAF-VPAF and AII), maintaining a segregation between parallel functional channels already established for the thalamocortical auditory interconnections. For the intrahemispheric connections, the analysis of the retrograde tracing data revealed that AAF and AI receive projections from the homolateral cortical areas PAF, VPAF and AII, whose neurons of origin were located mainly in their deep (V and VI) cortical layers. The reciprocal interconnections between the homolateral AAF and AI did not show a preferential laminar arrangement since the neurons of origin were distributed almost evenly in both superficial (II and III) and deep (V and VI) cortical layers. On the contrary, PAF received inputs from the homolateral cortical fields AAF, AI, AII and VPAF, originating predominantly from their superficial (II and III) layers. The homolateral projections reaching AII originated mainly from the superficial layers of AAF and AI, but from the deep layers of VPAF and PAF. The laminar distribution of anterogradely labeled terminal fields, when they were dense enough for a confident identification, was systematically related to the laminar arrangement of neurons of origin of the reciprocal projection: a projection originating from deep layers was associated with a reciprocal projection terminating mainly in layer IV, whereas a projection originating from superficial layers was associated with a reciprocal projection terminating predominantly outside layer IV. This laminar distribution indicates that the homolateral auditory cortical interconnections have a feed-forward/feed-back organization, corresponding to a hierarchical arrangement of the auditory cortical areas, according to criteria previously established in the visual system of primates. The principal auditory cortical areas could be ranked into 4 distinct hierarchical levels. The tonotopically organized areas AAF and AI represent the lowest level. The second level corresponds to the non-tonotopically organized area AII. Higher, the tonotopically organized areas VPAF and PAF occupy the third and fourth hierarchical levels, respectively.Abbreviations AAF anterior auditory cortical area - AI primary auditory cortical area - AII secondary auditory cortical area - BF best frequency - C cerebral cortex - CA caudate nucleus - CL claustrum - D dorsal nucleus of the dorsal division of the MGB - ea anterior ectosylvian sulcus - ep posterior ectosylviansulcus - IC internal capsule - LGN lateral geniculate nucleus - LV pars lateralis of the ventral division of the MGB - LVe lateral ventricule - M pars magnocellularis of the medial division of the MGB - MGB medial geniculate body - MGBv ventral division of the MGB - OT optic tract - OV pars ovoidea of the ventral division of the MGB - PAF posterior auditory cortical area - PH parahippocampal cortex - PO lateral part of the posterior group of thalamic nuclei - PU putamen - RE reticular complex of thalamus - rs rhinal sulcus - SG suprageniculate nucleus of the dorsal division of the MGB - ss suprasylvian sulcus - TMB tetrametylbenzidine - VBX ventrobasal complex - VLa ventrolateral complex - VL ventro-lateral nucleus of the ventral division of the MGB - WGA-HRP wheat germ agglutinin conjugated to horse-radish peroxidase - WM white matter - VPAF ventro-posterior auditory cortical area     

Cortical control of sound localization in the cat: unilateral cooling deactivation of 19 cerebral areas

We examined the ability of mature cats to accurately orient to, and approach, an acoustic stimulus during unilateral reversible cooling deactivation of primary auditory cortex (AI) or 1 of 18 other cerebral loci. After attending to a central visual stimulus, the cats learned to orient to a 100-ms broad-band, white-noise stimulus emitted from a central speaker or 1 of 12 peripheral sites (at 15 degrees intervals) positioned along the horizontal plane. Twenty-eight cats had two to six cryoloops implanted over multiple cerebral loci. Within auditory cortex, unilateral deactivation of AI, the posterior auditory field (PAF) or the anterior ectosylvian sulcus (AES) resulted in orienting deficits throughout the contralateral field. However, unilateral deactivation of the anterior auditory field, the second auditory cortex, or the ventroposterior auditory field resulted in no deficits on the orienting task. In multisensory cortex, unilateral deactivation of neither ventral or dorsal posterior ectosylvian cortices nor anterior or posterior area 7 resulted in any deficits. No deficits were identified during unilateral cooling of the five visual regions flanking auditory or multisensory cortices: posterior or anterior ii suprasylvian sulcus, posterior suprasylvian sulcus or dorsal or ventral posterior suprasylvian gyrus. In motor cortex, we identified contralateral orienting deficits during unilateral cooling of lateral area 5 (5L) or medial area 6 (6m) but not medial area 5 or lateral area 6. In a control visual-orienting task, areas 5L and 6m also yielded deficits to visual stimuli presented in the contralateral field. Thus the sound-localization deficits identified during unilateral deactivation of area 5L or 6m were not unimodal and are most likely the result of motor rather than perceptual impairments. Overall, three regions in auditory cortex (AI, PAF, AES) are critical for accurate sound localization as assessed by orienting.     

Auditory projections to extrastriate visual cortex: connectional basis for multisensory processing in ‘unimodal’ visual neurons

Neurophysiological studies have recently documented multisensory properties in ‘unimodal’ visual neurons of the cat posterolateral lateral suprasylvian (PLLS) cortex, a retinotopically organized area involved in visual motion processing. In this extrastriate visual area, a region has been identified where both visual and auditory stimuli were independently effective in activating neurons (bimodal zone), as well as a second region where visually-evoked activity was significantly facilitated by concurrent auditory stimulation but was unaffected by auditory stimulation alone (subthreshold multisensory region). Given their different distributions, the possible corticocortical connectivity underlying these distinct forms of crossmodal convergence was examined using biotinylated dextran amine (BDA) tracer methods in 21 adult cats. The auditory cortical areas examined included the anterior auditory field (AAF), primary auditory cortex (AI), dorsal zone (DZ), secondary auditory cortex (AII), field of the rostral suprasylvian sulcus (FRS), field anterior ectosylvian sulcus (FAES) and the posterior auditory field (PAF). Of these regions, the DZ, AI, AII, and FAES were found to project to the both the bimodal zone and the subthreshold region of the PLLS. This convergence of crossmodal inputs to the PLLS suggests not only that complex auditory information has access to this region but also that these connections provide the substrate for the different forms (bimodal versus subthreshold) of multisensory processing which may facilitate its functional role in visual motion processing.     

Topographical organization of the cortical afferent connections to the cortex of the anterior ectosylvian sulcus in the cat

Summary The cortical afferents to the cortex of the anterior ectosylvian sulcus (SEsA) were studied in the cat, using the retrograde axonal transport of horseradish peroxidase technique. Following injections of the enzyme in the cortex of both banks, fundus and both ends (postero-dorsal and anteroventral) of the anterior ectosylvian sulcus, retrograde labeling was found in: the primary, secondary, and tertiary somatosensory areas (SI, SII and SIII); the motor and premotor cortices; the primary, secondary, anterior and suprasylvian fringe auditory areas; the lateral suprasylvian (LS) area, area 20 and posterior suprasylvian visual area; the insular cortex and cortex of posterior half of the sulcus sylvius; in area 36 of the perirhinal cortex; and in the medial bank of the presylvian sulcus in the prefrontal cortex. Moreover, these connections are topographically organized. Considering the topographical distribution of the cortical afferents, three sectors may be distinguished in the cortex of the SEsA. 1) The cortex of the rostral two-thirds of the dorsal bank. This sector receives cortical projections from areas SI, SII and SIII, and from the motor cortex. It also receives projections from the anterolateral subdivision of LS, and area 36. 2) The cortex of the posterior third of the dorsal bank and of the posterodorsal end. It receives cortical afferents principally from the primary, secondary and anterior auditory areas, from SI, SII and fourth somatosensory area, from the anterolateral subdivision of LS, vestibular cortex and area 36. 3) The cortex of the ventral bank and fundus. This sulcal sector receives abundant connections from visual areas (LS, 20, posterior suprasylvian, 21 and 19), principally from the lateral posterior and dorsal subdivisions of LS. It also receives abundant connections from the granular insular cortex, caudal part of the cortex of the sylvian sulcus and suprasylvian fringe. Less abundant cortical afferents were found to arise in area 36, second auditory area and prefrontal cortex. The abundant sensory input of different modalities which appears to converge in the cortex of the anterior ectosylvian sulcus, and the consistent projection from this cortex to the deep layers of the superior colliculus, make this cortical region well suited to play a role in the control of the orientation movements of the eyes and head toward different sensory stimuli.Supported by FISSS grants 521/81 and 1250/84     

Connections of the anterior ectosylvian visual area (AEV)

Summary We have previously described a visual area situated in the cortex surrounding the deep infolding of the anterior ectosylvian sulcus of the cat (Mucke et al. 1982). Using orthograde and retrograde transport methods we now report anatomical evidence that this anterior ectosylvian visual area (AEV) is connected with a substantial number of both cortical and subcortical regions. The connections between AEV and other cortical areas are reciprocal and, at least in part, topographically organized: the rostral AEV is connected with the bottom region of the presylvian sulcus, the lower bank of the cruciate sulcus, the rostral part of the ventral bank of the splenial sulcus, the rostral portion of the lateral suprasylvian visual area (LS) and the lateral bank of the posterior rhinal sulcus; the caudal AEV is connected with the bottom region of the presylvian sulcus, the caudal part of LS, the ventral part of area 20 and the lateral bank of the posterior rhinal sulcus. Subcortically, AEV has reciprocal connections with the ventral medial thalamic nucleus (VM), with the medial part of the lateralis posterior nucleus (LPm), as well as with the lateralis medialis-suprageniculate nuclear (LM-Sg) complex. These connections are also topographically organized with more rostral parts of AEV being related to more ventral portions of the LPm and LM-Sg complex. AEV also projects to the caudate nucleus, the putamen, the lateral amygdaloid nucleus, the superior colliculus, and the pontine nuclei. It is concluded that AEV is a visual association area which functionally relates the visual with both the motor and the limbic system and that it might play a role in the animal's orienting and alerting behavior.Abbreviations Ac aqueductus cerebri - AEs anterior ectosylvian sulcus - ALLS anterolateral lateral suprasylvian area - AMLS anteromedial lateral suprasylvian area - ASs anterior suprasylvian sulcus - Cd caudate nucleus - CL central lateral nucleus - Cl claustrum - Cos coronal sulcus - Crs cruciate sulcus - DLS dorsal lateral suprasylvian area - GI stratum griseum intermediale - GP stratum griseum profundum - IC inferior colliculus - LAm lateral amygdaloid nucleus - LGNd dorsal nucleus of lateral geniculate body - LGNv ventral nucleus of lateral geniculate body - Llc nucleus lateralis intermedius, pars caudalis - LM nucleus lateralis medialis - LPl nucleus lateralis posterior, pars lateralis - LPm nucleus lateralis posterior, pars medialis - Ls lateral sulcus - MD nucleus mediodorsalis - MG medial geniculate body - MSs middle suprasylvian sulcus - Ndl nucleus dorsolateralis pontis - Nl nucleus lateralis pontis - Np nucleus peduncularis pontis - Npm nucleus paramedianus pontis - Nrt nucleus reticularis tegmenti pontis - Nv nucleus ventralis pontis - Ped cerebral peduncle - PEs posterior ectosylvian sulcus - Pg periaqueductal gray - PLLS posterolateral lateral suprasylvian area - PMLS posteromedial lateral suprasylvian area - PSs presylvian sulcus - Pul pulvinar - Put putamen - R red nucleus - Sg suprageniculate nucleus - SN substantia nigra - Sps splenial sulcus - Syls sylvian sulcus - T trapezoid body - VA ventral anterior nucleus - VL ventral lateral nucleus - VLS ventral lateral suprasylvian area - VM ventral medial nucleus - VPL ventral posterolateral nucleus - VPM ventral posteromedial nucleus Sponsored by Max-Planck-Society during part of the studySponsored by Thyssen FoundationSponsored by Alexander von Humboldt-Foundation     

Quantitative analyses of principal and secondary compound parieto-occipital feedback pathways in cat

The purpose of our study was to quantify the magnitude of principal and secondary pathways emanating from the middle suprasylvian (MS) region of visuoparietal cortex and terminating in area 18 of primary visual cortex. These pathways transmit feedback signals from visuoparietal cortex to primary visual cortex. (1) WGA-HRP was injected into area 18 to identify inputs from visual structures. In terms of numbers of neurons, feedback projections to area 18 from MS sulcal cortex (areas PMLS, AMLS and PLLS) comprise 26% of inputs from all visual structures. Of these neurons, between 21% and 34.9% are located in upper layers 2–4 and the dominant numbers are located in deep layers 5 and 6. Areas 17 (11.8%) and 19 (11.2%) provide more modest cortical inputs, and another eight areas provide a combined total of 4.3% of inputs. The sum of neurons in all subcompartments of the lateral geniculate nucleus (LGN) accounts for another 34.8% of the input to area 18, whereas inputs from the lateral division of the lateral-posterior nucleus (LPl) account for the final 11.9%. (2) Injection of tritiated-(³H)-amino acids into MS sulcal cortex revealed substantial direct projections from MS cortex that terminated in all layers of area 18, but with a markedly lower density in layer 4. Projections from MS cortex to both areas 17 and 19 are of similar density and characteristics, whereas those to other cortical targets have very low densities. Quantification also revealed minor-to-modest axon projections to all components of LGN and a massive projection throughout the LP-Pul complex. (3) Superposition of the labeled terminal and cell fields identified secondary, compound feedback pathways from MS cortex to area 18. The largest secondary pathway is massive and it includes the LPl nucleus. Much more modest secondary pathways include areas 17 and 19, and LGN. The relative magnitudes of the secondary pathways suggest that the one through LPl exerts a major influence on area 18, whereas the others exert more modest or minor influences. MS cortex in the contralateral hemisphere also innervates area 18 directly. These data are important for interpreting the impact of deactivating feedback projections from visuoparietal cortex on occipital cortex.Abbreviations A layer A of LGN - A1 layer A1 of LGN - ALLS anterolateral visual area of the lateral suprasylvian sulcus (Palmer et al. 1978) - AMLS anteromedial visual area of the lateral suprasylvian sulcus (Palmer et al. 1978) - Aud auditory cortex of the middle ectosylvian gyrus - CC corpus callosum - Cg cingulate gyrus - Cm magnocellular layers of LGN - Cp parvocellular layers of LGN - LGN dorsal lateral geniculate nucleus - LP lateral posterior nucleus - LPl lateral division of the lateral posterior nucleus - LPm medial division of the lateral posterior nucleus (Graybiel and Berson 1980, Berson and Graybiel 1978; Raczkowski and Rosenquist 1983) - MIN medial interlaminar nucleus subdivision of LGN - MS cortex bounding the middle suprasylvian sulcus (areas AMLS, ALLS, PMLS, and PLLS) - OR optic radiation - PE posterior ectosylvian visual cortex - PLLS posterolateral visual area of the lateral suprasylvian sulcus (Palmer et al. 1978) - PMLS posteromedial visual area of the lateral suprasylvian sulcus (Palmer et al. 1978) - Pul pulvinar nucleus - SVA splenial visual area - V1 primary visual cortex - V2 secondary visual cortex - V3 third visual area - V5/MT fifth visual area/middle temporal area - WGA-HRP wheat germ agglutinin conjugated to horseradish peroxidase - Wing wing of LGN - 7 area 7 - 17 area 17 - 18 area 18 - 19 area 19     

The association connexions of the suprasylvian fringe (SF) and other areas of the cat auditory cortex

The association connexions of the peri-auditory (SF, Ea and INS) and auditory (AI, AII and Ep) areas of the cat cortex were studied in silver impregnated material of 32 experiments with cortical lesions. The cortex of the lateral bank of the rostral part of the middle suprasylvian sulcus (SF) sends many fibres to AI and to the insular cortex (INS), and has scanty projections upon AII and Ep. In addition, it sends fibres to the visual area 17 as well as to the ventral bank of the medial part of the cruciate sulcus. It receives fibres from the three auditory areas AI, AII and Ep, as well as from Ea and INS. The dorsal part of the anterior ectosylvian gyrus (Ea) projects upon SF, AI, and AII. Ea sends few fibres to Ep, and receives relatively dense projections from AI and AII. The anterior sylvian gyrus (INS) projects heavily upon AII as well as upon the superficial part of SF. It sends a few fibres also to Ep. INS receives heavy projections from AII and relatively lighter connections from SF, AI and Ep. The three auditory areas AI, AII and Ep are strongly mutually interconnected. AI and Ep have scanty projections upon the visual area 19, and AI also to the lateral suprasylvian visual area, as well as upon the ventral bank of the medial cruciate sulcus. Correlations of the association connexions with the functions of each area are discussed.     

Sound localization during homotopic and heterotopic bilateral cooling deactivation of primary and nonprimary auditory cortical areas in the cat

Although the contributions of primary auditory cortex (AI) to sound localization have been extensively studied in a large number of mammals, little is known of the contributions of nonprimary auditory cortex to sound localization. Therefore the purpose of this study was to examine the contributions of both primary and all the recognized regions of acoustically responsive nonprimary auditory cortex to sound localization during both bilateral and unilateral reversible deactivation. The cats learned to make an orienting response (head movement and approach) to a 100-ms broad-band noise stimulus emitted from a central speaker or one of 12 peripheral sites (located in front of the animal, from left 90 degrees to right 90 degrees , at 15 degrees intervals) along the horizontal plane after attending to a central visual stimulus. Twenty-one cats had one or two bilateral pairs of cryoloops chronically implanted over one of ten regions of auditory cortex. We examined AI [which included the dorsal zone (DZ)], the three other tonotopic fields [anterior auditory field (AAF), posterior auditory field (PAF), ventral posterior auditory field (VPAF)], as well as six nontonotopic regions that included second auditory cortex (AII), the anterior ectosylvian sulcus (AES), the insular (IN) region, the temporal (T) region [which included the ventral auditory field (VAF)], the dorsal posterior ectosylvian (dPE) gyrus [which included the intermediate posterior ectosylvian (iPE) gyrus], and the ventral posterior ectosylvian (vPE) gyrus. In accord with earlier studies, unilateral deactivation of AI/DZ caused sound localization deficits in the contralateral field. Bilateral deactivation of AI/DZ resulted in bilateral sound localization deficits throughout the 180 degrees field examined. Of the three other tonotopically organized fields, only deactivation of PAF resulted in sound localization deficits. These deficits were virtually identical to the unilateral and bilateral deactivation results obtained during AI/DZ deactivation. Of the six nontonotopic regions examined, only deactivation of AES resulted in sound localization deficits in the contralateral hemifield during unilateral deactivation. Although bilateral deactivation of AI/DZ, PAF, or AES resulted in profound sound localization deficits throughout the entire field, the cats were generally able to orient toward the hemifield that contained the acoustic stimulus, but not accurately identify the location of the stimulus. Neither unilateral nor bilateral deactivation of areas AAF, VPAF, AII, IN, T, dPE, nor vPE had any effect on the sound localization task. Finally, bilateral heterotopic deactivations of AI/DZ, PAF, or AES yielded deficits that were as profound as bilateral homotopic cooling of any of these sites. The fact that deactivation of any one region (AI/DZ, PAF, or AES) was sufficient to produce a deficit indicated that normal function of all three regions was necessary for normal sound localization. Neither unilateral nor bilateral deactivation of AI/DZ, PAF, or AES affected the accurate localization of a visual target. The results suggest that hemispheric deactivations contribute independently to sound localization deficits.     

Physiologic and anatomic investigation of a visual cortical area situated in the ventral bank of the anterior ectosylvian sulcus of the cat

Summary In this paper a cortical area is described that covers approximately the posterior two-thirds of the ventral bank of the anterior ectosylvian sulcus of the cat and is called anterior ectosylvian visual area (AEV).In cats anesthetized with a combination of N₂O and barbiturate we explored this area by recording extracellularly the responses of AEV neurons to visual and electric stimulation as well as by injecting HRP into physiologically verified points. AEV neurons were found to be highly sensitive to small light stimuli moving rapidly in a particular direction through their large receptive fields. The properties of 74 neurons were quantitatively analyzed. Increasing the length of the stimulus within the receptive field to more than 2 deg strongly inhibited the responses, whereas increasing the speed of the stimulus movement up to 72–120 deg/s enhanced the neuronal responsiveness. Although the majority of neurons responded to a wide range of possible directions, one clearly preferred direction could usually be found for each neuron. There was a predominance of preferred directions toward the contralateral hemifield. Anatomic and electrophysiologic connectivity studies showed that AEV receives its main afferent inputs from the lateral suprasylvian visual area (LS) and from the tecto-recipient zone of the nucleus lateralis posterior (LP)-pulvinar complex.Although these studies suggested some topographical organization within the projection from LS to AEV, the large receptive fields in AEV, the great majority of which included the central area, did not reveal a clear retinotopic order. It is concluded that AEV is a specific visual area and that functionally the extrageniculate inputs predominate.Abbreviations AEs anterior ectosylvian sulcus - ALLS anterolateral lateral suprasylvian area - AMLS anteromedial lateral suprasylvian area; - Cl Claustrum - DLS dorsal lateral suprasylvian area - LGNd dorsal nucleus of lateral geniculate body - LGNv ventral nucleus of lateral geniculate body - LM nucleus lateralis medialis - LP1a nucleus lateralis posterior, pars lateralis - LPm nucleus lateralis posterior, pars medialis - Ls lateral sulcus - MGmc magnocellular division of medial geniculate body - MGpc parvocellular division of medial geniculate body - MSs middle suprasylvian sulcus - NP nucleus posterior of Rioch - PLLS postero-lateral lateral suprasylvian area - PLs posterolateral sulcus - PMLS posteromedial lateral suprasylvian area - Pu putamen - Pul pulvinar - Sg suprageniculate nucleus - VLS ventral lateral suprasylvian area Sponsored by Max-Planck-Gesellschaft and IBRODept. of Anatomy, School of Medicine, Iwate Medical University, Morioka 020, JapanSponsored by Alexander von Humboldt-FoundationDept. of Physiology, University Medical School, Szeged, Hungary     

Several neuronal and axonal types form long intrinsic connections in the cat primary auditory cortical field (AI)

Intrinsic connections in the cat primary auditory field (AI) as revealed by injections Phaseolus vulgaris leucoagglutinin (PHA-L) or biocytin, had an anisotropic and patchy distribution. Neurons, labelled retrogradely with PHA-L were concentrated along a dorsoventral stripe through the injection site and rostral to it; the spread of rostrally located neurons was greater after injections into regions of low rather than high characteristic frequencies. The intensity of retrograde labelling varied from weak and granular to very strong and Golgi-like. Out of 313 Golgi like retrogradely labelled neurons 79.6% were pyramidal, 17.2% multipolar, 2.6% bipolar, and 0.6% bitufted; 13.4% were putatively inhibitory, i.e. aspiny or sparsely spiny multipolar, or bitufted. Individual anterogradely labelled intrinsic axons were reconstructed for distances of 2 to 7 mm. Five main types were distinguished on the basis of the branching pattern and the location of synaptic specialisations. Type 1 axons travelled horizontally within layers II to VI and sent collaterals at regular intervals; boutons were only present in the terminal arborizations of these collaterals. Type 2 axons also travelled horizontally within layers II to VI and had rather short and thin collateral branches; boutons or spine-like protrusions occurred in most parts of the axon. Type 3 axons travelled obliquely through the cortex and formed a single terminal arborization, the only site where boutons were found. Type 4 axons travelled for some distance in layer I; they formed a heterogeneous group as to their collaterals and synaptic specializations. Type 5 axons travelled at the interface between layer VI and the white matter; boutons en passant, spine-like protrusions, and thin short branches with boutons en passant were frequent all along their trajectory. Thus, only some axonal types sustain the patchy pattern of intrinsic connectivity, whereas others are involved in a more diffuse connectivity.Abbreviations AAF anterior auditory cortical field - AI primary auditory cortical field - AII secondary auditory cortical field - ALLS anterolateral lateral suprasylvian visual area - CF characteristic frequency - IFL isofrequency line - INJ injection - LV pars lateralis of the ventral division of the MGB - MGB medial geniculate body - mss middle suprasylvian sulcus - OV pars ovoidea of the ventral division of the MGB - PAF posterior auditory field - PHA-L Phaseolus vulgaris leucoagglutinin - PO posterior nucleus of the thalamus - R rostral - SF suprasylvian fringe - syl sylvian sulcus - TBS TRIS-buffered saline - V ventral - VL ventro-lateral nucleus of the MGB     

The laminar distribution of cortical connections with the tecto- and cortico-recipient zones in the cat's lateral posterior nucleus

The anterograde and retrograde transport of wheat germ agglutinin congugated to horseradish peroxidase was used to examine the laminar organization of cortical connections with the two visual zones that comprise the cat's lateral posterior nucleus. Microelectrophoretic deposits of the tracer into the principal tecto-recipient zone in the medial division of the lateral posterior nucleus revealed reciprocal connections with the following cortical fields: areas 19 and 21a, the medial and lateral banks of the middle suprasylvian sulcus, and the dorsal and ventral banks of the lateral suprasylvian sulcus, which correspond to the dorsal lateral suprasylvian and ventral lateral suprasylvian visual areas of Palmer et al. [(1978) Brain Res. 177, 237-256] and an area in the fundus of the posterior suprasylvian sulcus. In each of these cortical areas two distinct populations of cells were labeled, small pyramidal neurons in layer VI and large pyramidal cells in layer V. Overlying these backfilled cells were two bands of anterograde label, a narrow strip in layer I and a wide band centered in layer IV. Deposits of wheat germ agglutinin conjugated to horseradish peroxidase confined to the striate-recipient zone in the lateral portion of the lateral posterior nucleus resulted in cortical label in areas 17, 18, 19, 20a and b, 21a, the medial and lateral banks of the middle suprasylvian sulcus, the posterior suprasylvian sulcus and in the fundus of the splenial sulcus. In all cortical areas other than 17 and 18, the laminar distribution of label was the same as that found after deposits of the tracer into the medial division of the lateral posterior nucleus. In contrast, areas 17 and 18 contained backfilled cells that were confined to layer V and anterograde label that was restricted to layer I. These findings indicate that the cortical areas that receive a direct projection from the A laminae of the dorsal lateral geniculate nucleus maintain a distinct laminar organization of reciprocal connections with the extrageniculate visual thalamus. Conversely, all other visual areas of the cortex share a common pattern of reciprocal connections with both the tecto- and striate-recipient zones of the lateral posterior nucleus.     

Afferent fibers to the anterior suprasylvian gyrus from the medial geniculate body of cat

Afferents to the anterior suprasylvian gyrus (ASG) from the medial geniculate body of cat were demonstrated by means of autoradiography. [3H]Glycine was injected stereotactically into the medial division of the medial geniculate body (mMGB). After a 3-day survival period, the auditory cortices and the ASG were excised. Labelled terminals were found in the ASG, in the anterior auditory field (AAF) and in the acoustic cortex (AI). The density of labelling was highest in the ASG and lower in the AAF and AI. The afferents from the mMGB made synaptic contacts in the 3rd layer of the cortices examined.     

Cortical inputs to the CA1 field of the monkey hippocampus originate from the perirhinal and parahippocampal cortex but not from area TE.

We determined the cortical regions that project directly to the CA1 field of the monkey hippocampus by injecting the retrograde tracers Fast blue, Diamidino yellow or WGA-HRP into CA1 and examining the distribution of labeled cells. In the temporal lobe, large numbers of retrogradely labeled cells were observed in the perirhinal and parahippocampal cortices. Only an occasional labeled cell, however, was observed in the unimodal visual area TE. Additional projections to CA1 arose in the dorsal bank of the superior temporal sulcus, in the rostral and retrosplenial portions of the cingulate cortex, in the agranular insular cortex, and in the caudal orbitofrontal cortex.     

Branching cortical neurons in cat which project to the colliculi and to the pons: a retrograde fluorescent double-labeling study

Summary The fluorescent double-labeling technique has been used to determine whether the corticopontine and the corticotectal fibers in the cat are derived from two different sets of neurons or whether they are derived from branching neurons which distribute collaterals to the pontine grey and the colliculi. After unilateral DY.2HCl injections in the pontine grey and FB injections in the ipsilateral colliculi, large numbers of FB-DY.2HCl double-labeled neurons were present in the cortex of the ipsilateral hemisphere. However, the labeled neurons in its rostral part may have represented pyramidal tract neurons which were labeled retrogradely because their fibers descended through the DY.2HCl injection area. Therefore, also DY.2HCl injections were made in the pyramid (i.e. caudal to the pons) and the cortical pyramidal tract area, containing the retrograde DY.2HCl-labeled neurons, was delineated. In the rest of the experiments only the DY.2HCl-labeled neurons in the caudal two thirds of the hemisphere (outside the pyramidal tract area) were taken into account because only these neurons could, with confidence, be regarded as corticopontine neurons. In some anterograde HRP transport experiments the trajectories of the corticotectal and the corticopontine fibers were visualized. On the basis of the findings the DY.2HCl injections in the pontine grey were placed such that they could not involve any of the corticotectal fibers passing from the cerebral peduncle to the colliculi. Thus artifactual doublelabeling of cortical neurons was avoided. However, also under these circumstances many double-labeled neurons were present in the caudal two thirds of the hemisphere. This led to the conclusion that in the cat a large proportion of the corticopontine neurons in the caudal two thirds of the hemisphere represent branching neurons which also distribute collaterals to the colliculi. The parietal (anterior part of the lateral gyrus, middle and posterior suprasylvian gyri) and the cingulate areas together contained three quarters of all labeled corticopontine neurons outside the pyramidal tract area. In the parietal areas roughly 25% of them were double-labeled and in the cingulate area 14%. However, in the visual areas 18 and 19 a much larger percentage (30–60%) was doublelabeled. In a recent study from our laboratory it was found that in the cat the pyramidal tract fibers distribute an abundance of collaterals to the pontine grey. Therefore, a large proportion of all corticopontine connections in this species appear to be established by branching neurons which also distribute fibers to other cell groups in the brain stem and the spinal cord.Abbreviations A.E. anterior ectosylvian sulcus - a.e.s. anterior ectosylvian sulcus - BC brachium conjunctivum - BCI brachium colliculus inferior - BP brachium pontis - cor. sulc. coronal sulcus - CP cerebral peduncle - CR. cruciate sulcus - CUN cuneiform nucleus - DBC decussation brachium conjunctivum - DLP dorsolateral pontine nucleus - IC inferior colliculus - inf. coll. inferior colliculus - INS. insula cortex - IO inferior olive - IP interpeduncular nucleus - LAT. lateral sulcus - l.s. lateral sulcus - MG medial geniculate body - LL lateral lemniscus - ML medial lemniscus - MLF medial longitudinal fascicle - NdG dorsal nucleus of Gudden - NLL nucleus lateral lemniscus - NRTP reticular tegmental pontine nucleus - ORB. orbital sulcus - P pyramid - PAG periaqueductal grey - P.E. posterior ectosylvian sulcus - RF reticular formation - PG pontine grey - RB restiform body - RN red nucleus - S. sylvian sulcus - SC superior colliculus - SN substantia nigra - SO superior olive - SPV spinal trigeminal complex - S.S. suprasylvian sulcus - s.syl.s. suprasylvian sulcus - S.SPL. suprasplenial sulcus - SPL. splenial sulcus - spl.s. splenial sulcus - sup. coll. superior colliculus - syl.s. sylvian sulcus - TB trapezoid body - VC vestibular complex - Vm trigeminal motor nucleus - Vs trigeminal principle nucleus - III oculomotor nucleus - IV trochlear nucleus - VI abducens nucleus - VII facial nerve - VIII vestibulo-trochlear nerve Supported in part by grant 13-46-91 of FUNGO/ZWO (Dutch Organization for Fundamental Research in Medicine)     

Branched projections in the auditory thalamocortical and corticocortical systems

Branched axons (BAs) projecting to different areas of the brain can create multiple feature-specific maps or synchronize processing in remote targets. We examined the organization of BAs in the cat auditory forebrain using two sensitive retrograde tracers. In one set of experiments (n=4), the tracers were injected into different frequency-matched loci in the primary auditory area (AI) and the anterior auditory field (AAF). In the other set (n=4), we injected primary, non-primary, or limbic cortical areas. After mapped injections, percentages of double-labeled cells (PDLs) in the medial geniculate body (MGB) ranged from 1.4% (ventral division) to 2.8% (rostral pole). In both ipsilateral and contralateral areas AI and AAF, the average PDLs were <1%. In the unmapped cases, the MGB PDLs ranged from 0.6% (ventral division) after insular cortex injections to 6.7% (dorsal division) after temporal cortex injections. Cortical PDLs ranged from 0.1% (ipsilateral AI injections) to 3.7% in the second auditory cortical area (AII) (contralateral AII injections). PDLs within the smaller (minority) projection population were significantly higher than those in the overall population. About 2% of auditory forebrain projection cells have BAs and such cells are organized differently than those in the subcortical auditory system, where BAs can be far more numerous. Forebrain branched projections follow different organizational rules than their unbranched counterparts. Finally, the relatively larger proportion of visual and somatic sensory forebrain BAs suggests modality specific rules for BA organization.     

Deoxyglucose uptake in the ferret auditory cortex

Histological methods and 2-deoxyglucose autoradiography were used in an attempt at finding distinguishing characteristics that would permit the clear definition of different auditory areas on the ectosylvian gyrus. This region was studied in both coronal and flattened tangential sections. In tangential sections a crescent-shaped region of high deoxyglucose uptake was identified. The centre of this crescent was in the position of the primary auditory area on the middle ectosylvian gyrus. The ventro-anterior arm of the crescent was on the surface of the anterior ectosylvian gyrus and the ventro-posterior arm on the posterior ectosylvian gyrus. All three parts of the crescent appear to have an auditory function, because ablating the inferior colliculus or inserting a contralateral earplug reduced their deoxyglucose uptake. This was shown by using two separately distinguishable forms of 2-deoxyglucose, incorporating the ¹⁸F and ¹⁴C isotopes. In addition, another area of high deoxyglucose activity was identified in the ventral wall of the suprasylvian sulcus, which seems to correspond to the anterior auditory field. These four areas with high deoxyglucose uptake also have high levels of succinate dehydrogenase activity and moderately high densities of myelinated fibres. Succinate dehydrogenase histochemistry provides a simple method for identifying auditory cortical areas and should be of use in future physiological studies. These results provide evidence that the ferret has four separate auditory areas with relatively high metabolic and functional activity. Received: 8 August 1996 / Accepted: 15 May 1997     

Multiparametric auditory receptive field organization across five cortical fields in the albino rat

The auditory cortex of the rat is becoming an increasingly popular model system for studies of experience-dependent receptive field plasticity. However, the relative position of various fields within the auditory core and the receptive field organization within each field have yet to be fully described in the normative case. In this study, the macro- and micro-organizational features of the auditory cortex were studied in pentobarbital-anesthetized adult rats with a combination of physiological and anatomical methods. Dense microelectrode mapping procedures were used to identify the relative position of five tonotopically organized fields within the auditory core: primary auditory cortex (AI), the posterior auditory field (PAF), the anterior auditory field (AAF), the ventral auditory field (VAF), and the suprarhinal auditory field (SRAF). AI and AAF both featured short-latency, sharply tuned responses with predominantly monotonic intensity-response functions. SRAF and PAF were both characterized by longer-latency, broadly tuned responses. VAF directly abutted the ventral boundary of AI but was almost exclusively composed of low-threshold nonmonotonic intensity-tuned responses. Dual injection of retrograde tracers into AI and VAF was used to demonstrate that the sources of thalamic input from the medial geniculate body to each area were essentially nonoverlapping. An analysis of receptive field parameters beyond characteristic frequency revealed independent spatially ordered representations for features related to spectral tuning, intensity tuning, and onset response properties in AI, AAF, VAF, and SRAF. These data demonstrate that despite its greatly reduced physical scale, the rat auditory cortex features a surprising degree of organizational complexity and detail.     

Auditory cortex projections target the peripheral field representation of primary visual cortex

The purpose of the present study was to identify projections from auditory to visual cortex and their organization. Retrograde tracers were used to identify the sources of auditory cortical projections to primary visual cortex (areas 17 and 18) in adult cats. Two groups of animals were studied. In the first group, large deposits were centered on the lower visual field representation of the vertical meridian located along the area 17 and 18 border. Following tissue processing, characteristic patterns of cell body labeling were identified in extrastriate visual cortex and the visual thalamus (LGN, MIN, & LPl). In auditory cortex, of the four tonotopically-organized regions, neuronal labeling was identified in the supragranular layers of the posterior auditory field (PAF). Little to no labeling was evident in the primary auditory cortex, the anterior auditory field, the ventral posterior auditory field or in the remaining six non-tonotopically organized regions of auditory cortex. In the second group, small deposits were made into the central or peripheral visual field representations of primary visual cortex. Labeled cells were identified in PAF following deposits into regions of primary visual cortex representing peripheral, but not central, visual field representations. Furthermore, a coarse topography was identified in PAF, with neurons projecting to the upper field representation being located in the gyral portion of PAF and neurons projecting to the lower field representation located in the sulcal portion of PAF. Therefore, direct projections can be identified from tonotopically organized auditory cortex to the earliest stages of visual cortical processing.     

Projections of the pulvinar-lateral posterior complex to visual cortical areas in the cat

The projections of the pulvinar-lateral posterior complex of the cat were studied using the autoradiographic tracing method and related to 15 previously defined cortical areas. The results indicate that each of three separate zones within the pulvinar-lateral posterior complex has a different pattern of projection. The most lateral zone, the pulvinar, sends fibers to at least seven cortical areas, most of which are known to have input from other visual areas within the brain: the splenial visual area, the cingulate gyrus, and areas 5, 7, 19, 20a and 21a. A zone located just medial to the pulvinar, the lateral division of the lateral posterior complex, projects to at least eight visual areas in the cortex: areas 17, 18, 19, 20a, 21a, 21b, the posteromedial lateral suprasylvian area and the ventral lateral suprasylvian area. The most medial zone, the intermediate division of the lateral posterior complex, projects to at least four cortical areas: 20a, the posterior suprasylvian area, the posterolateral lateral suprasylvian area and the dorsal lateral suprasylvian area. Of the 15 cortical areas that receive fibers from the pulvinar-lateral posterior complex, only three (areas 19, 20a and 21a) receive projections from more than one of these thalamic zones, and only one of the cortical areas (20a) receives fibers from all three zones.Thus, the data support the division of the pulvinar lateral posterior complex into three zones on the basis of their unique and largely non-overlapping projections to the visual cortex.     

Postnatal development of calbindin-D28k immunoreactivity in the cerebral cortex of the cat

To learn about maturational patterns of nonpyramidal neurons in the cerebral cortex, calbindin-D28k immunoreactivity was studied in the kitten cortex. Immunoreactive neurons first appear in the cortical and subcortical areas related to the limbic system, including the cingulate and retrosplenial cortices, and in the secondary motor areas. These are followed by the primary motor and sensory association areas and, finally, by the primary sensory areas. In all cortical areas, calbindin-D28k immunoreactivity first develops in layer V pyramidal neurons and later in nonpyramidal neurons, except in the primary sensory areas, where immunoreactive pyramidal neurons are not found at any age. Transient calbindin-D28k immunoreactivity occurs in pyramidal neurons that are mainly localized in the cingulate and retrosplenial cortices and in the secondary motor area, as well as in nonpyramidal neurons localized in the subplate and layer I, and in a subset of large multipolar and bitufted neurons in layer VI. Nonpyramidal neurons localized in layers II to IV, and some neurons in layer VI, develop permanent calbindin-D28k immunoreactivity. Calbindin-D28k immunoreactivity labels subsets of GABAergic interneurons that form vertical axonal tufts, so that temporal and regional patterns of calbindin-D28k immunoreactivity during development may be implicated in the maturation of columnar (vertical) inhibition in the cerebral cortex. In addition to neurons, corticofugal and afferent fibres of subcortical origin exhibit calbindin-D28k immunoreactivity. Transient calbindin-D28k immunoreactivity occurs in corticofugal fibres arising from the cingulate and prefrontal cortices, which are probably corticostriatal projection fibres. In contrast, permanent immunoreactivity occurs in what are probably thalamocortical fibres ending in layer IV, and in punctate terminals located in the upper third of layer I.Abbreviations AI Auditory area I - AA anterior auditory field - CG cingulate cortex - CL claustrum - CN caudate nucleus - COR sulcus coronarius - CP cortical plate - CRU sulcus cruciatus - EC entorhinal cortex - ECSA sulcus ectosylvius anterior - GABA gamma-aminobutyric acid - HP hippocampus - IC internal capsule - INS insular cortex - LAT sulcus lateralis - LGN lateral geniculate nucleus - MI primary motor area - MII supplementary motor area - PIR cortex piriformis - PLLS posterolateral lateral suprasylvian visual area - PMLS posteromedial lateral suprasylvian visual area - PRS sulcus praesylvius - PU putamen - RAN sulcus rhinicus anterior - SI somatosensory area I - SII somatosensory area II - SCC sulcus corporis callosi - SEP septum - SIL sulcus cerebri lateralis - SP subplate - SPL sulcus splenialis - SSPL sulcus suprasplenialis - SUPS sulcus suprasylvius - T thalamus - TE temporal auditory area - WM white matter - 7 association area 7 - 17 primary visual area 17 - 18 visual area 18 - 19 visual area 19