"Ventral" area in the rat auditory cortex: a major auditory field connected with the dorsal division of the medial geniculate body

The rat auditory cortex is made up of multiple auditory fields. A precise correlation between anatomical and physiological areal extents of auditory fields, however, is not yet fully established, mainly because non-primary auditory fields remain undetermined. In the present study, based on thalamocortical connection, electrical stimulation and auditory response, we delineated a non-primary auditory field in the cortical region ventral to the primary auditory area and anterior auditory field. We designated it as "ventral" area after its relative location. At first, based on anterograde labeling of thalamocortical projection with biocytin, ventral auditory area was delineated as a main cortical terminal field of thalamic afferents that arise from the dorsal division of the medial geniculate body. Cortical terminal field (ventral auditory area) extended into the ventral margin of temporal cortex area 1 (Te1) and the dorsal part of temporal cortex area 3, ventral (Te3V), from 3.2-4.6 mm posterior to bregma. Electrical stimulation of the dorsal division of the medial geniculate body; evoked epicortical field potentials confined to the comparable cortical region. On the basis of epicortical field potentials evoked by pure tones, best frequencies were further estimated at and around the cortical region where electrical stimulation of the dorsal division of the medial geniculate body evoked field potentials. Ventral auditory area was found to represent frequencies primarily below 15 kHz, which contrasts with our previous finding that the posterodorsal area, the other major recipient of the dorsal division of the medial geniculate body; projection, represents primarily high frequencies (>15 kHz). The posterodorsal area is thought to play a pivotal role in auditory spatial processing [Kimura A, Donishi T, Okamoto K, Tamai Y (2004) Efferent connections of "posterodorsal" auditory area in the rat cortex: implications for auditory spatial processing. Neuroscience 128:399-419]. The ventral auditory area, as the other main cortical region that would relay auditory input from the dorsal division of the medial geniculate body to higher cortical information processing, could serve an important extralemniscal function in tandem with the posterodorsal area. The results provide insight into structural and functional organization of the rat auditory cortex.     

Auditory thalamic nuclei projections to the temporal cortex in the rat

Thalamocortical projections from the auditory thalamic nuclei were examined systematically in the rat, including those from the dorsal division (MGD) of the medial geniculate body (MG), which were less clearly determined in previous studies. Injections of biocytin confined in each thalamic nucleus revealed characteristic features of projections in terms of cortical areas and layers of termination. In contrast to exclusively selective projections to cortical area Te1 from the ventral division (MGV) of the MG, diffuse and selective terminations were observed in the projections from the dorsal (MGD) and medial divisions (MGM) of the MG and the suprageniculate nucleus (SG). Diffuse termination was continuous in layer I or VI of the temporal cortex, while selective termination was in layers III and IV of discrete cortical areas. In addition to diffuse termination in the upper half of layer I of cortical areas Te1, Te2d and Te3v, the MGD and SG projections formed plexuses of axons selectively in lower layer III and layer IV of Te2d and Te3v. The SG projections targeted further the dorsal bank of the perirhinal cortex (PRh), while the MGD projections targeted in part the ventral fringe of Te1. The MGM projections terminated diffusely in layer VI of Te1 and Te3v, and selectively in lower layer III and layer IV of the rostral part of Te3v. Diffuse projections to layers I and VI from the SG and MGM extended in cortical regions over the dorsal fringe of Te1. Selective dense projections to middle cortical layers of Te2d and Te3v (especially its rostral part) indicate the existence of auditory areas, which could be involved in cross-modal interaction with visual and somatosensory system, respectively. Diffuse projections are supposed to bind information processings in these areas and the primary auditory area (Te1).     

Cytoarchitecture of the medial geniculate body and thalamic projections to the auditory cortex in the rufous horseshoe bat (Rhinolophus rouxi). I. Temporal fields

The auditory cortex in echolocating bats is one of the best studied in mammals, yet the projections of the thalamus to the different auditory cortical fields have not been systematically analyzed in any bat species. The data of the present study were collected as part of a combined investigation of physiological properties, neuroarchitecture, and chemoarchitecture as well as connectivity of cortical fields in Rhinolophus in order to establish a neuroanatomically and functionally coherent view of the auditory cortex in the horseshoe bat. This paper first describes the neuroanatomic parcellation of the medial geniculate body and then concentrates on the afferent thalamic connections with auditory cortical fields of the temporal region. Deposits of horseradish peroxidase and wheatgerm-agglutinated horseradish peroxidase were made into neurophysiologically characterized locations of temporal auditory cortical fields; i.e., the tonotopically organized primary auditory cortex, a ventral field, and a temporal subdivision of a posterior dorsal field. A clear topographic relationship between thalamic subdivisions and specific cortical areas is demonstrated. The primary auditory cortex receives topographically organized input from the central ventral medial geniculate body. The projection patterns to the temporal subdivision of the posterior dorsal field suggest that it is a "core" field, similar to the posterior fields in the cat. Projections to the ventral field arise primarily from border regions of the ventral medial geniculate body. On the whole, the organization of the medial geniculate body projections to the temporal auditory cortex is quite similar to that described in other mammals, including cat and monkey.     

Cytoarchitecture of the medial geniculate body and thalamic projections to the auditory cortex in the rufous horseshoe bat (<Emphasis Type="Italic">Rhinolophus rouxi)</Emphasis>

The auditory cortex in echolocating bats is one of the best studied in mammals, yet the projections of the thalamus to the different auditory cortical fields have not been systematically analyzed in any bat species. The data of the present study were collected as part of a combined investigation of physiological properties, neuroarchitecture, and chemoarchitecture as well as connectivity of cortical fields in Rhinolophus in order to establish a neuroanatomically and functionally coherent view of the auditory cortex in the horseshoe bat. This paper first describes the neuroanatomic parcellation of the medial geniculate body and then concentrates on the afferent thalamic connections with auditory cortical fields of the temporal region. Deposits of horseradish peroxidase and wheatgerm-agglutinated horseradish peroxidase were made into neurophysiologically characterized locations of temporal auditory cortical fields; i.e., the tonotopically organized primary auditory cortex, a ventral field, and a temporal subdivision of a posterior dorsal field. A clear topographic relationship between thalamic subdivisions and specific cortical areas is demonstrated. The primary auditory cortex receives topographically organized input from the central ventral medial geniculate body. The projection patterns to the temporal subdivision of the posterior dorsal field suggest that it is a “core” field, similar to the posterior fields in the cat. Projections to the ventral field arise primarily from border regions of the ventral medial geniculate body. On the whole, the organization of the medial geniculate body projections to the temporal auditory cortex is quite similar to that described in other mammals, including cat and monkey.     

Thalamic projections to the auditory cortex in the rufous horseshoe bat (Rhinolophus rouxi). II. Dorsal fields

In this study, we analyzed the thalamic connections to the parietal or dorsal auditory cortical fields of the horseshoe bat, Rhinolophus rouxi. The data of the present study were collected as part of a combined investigation of physiologic properties, neuroarchitecture, and chemoarchitecture as well as connectivity of cortical fields in Rhinolophus, in order to establish a neuroanatomically and functionally coherent view of the auditory cortex. Horseradish peroxidase or wheat-germ-agglutinated horseradish peroxidase deposits were made into cortical fields after mapping response properties. The dorsal fields of the auditory cortex span nearly the entire parietal region and comprise more than half of the non-primary auditory cortex. In contrast to the temporal fields of the auditory cortex, which receive input mainly from the ventral medial geniculate body (or "main sensory nucleus"), the dorsal fields of the auditory cortex receive strong input from the "associated nuclei" of the medial geniculate body, especially from the anterior dorsal nucleus of the medial geniculate body. The anterior dorsal nucleus is as significant for the dorsal fields of the auditory cortex as the ventral nucleus of the medial geniculate body is for the temporal fields of the auditory cortex. Additionally, the multisensory nuclei of the medial geniculate body provide a large share of the total input to the nonprimary fields of the auditory cortex. Comparing the organization of thalamic auditory cortical afferents in Rhinolophus with other species demonstrates the strong organizational similarity of this bat's auditory cortex with that of other mammals, including primates, and provides further evidence that the bat is a relevant and valuable model for studying mammalian auditory function.     

Topography of corticothalamic projections from the auditory cortex of the rat

Corticothalamic projections from cortical auditory field to the medial geniculate body (MG) in the rat were systematically examined by making small injections of biocytin in cortical area Te1. All injections, confined to 400 microm in diameter, resulted in two projections terminating in the ventral (MGV) and dorsal divisions (MGD) of the MG. The projections to the MGV were evidently topographic. The rostral and caudal portions of area Te1 projected to the ventromedial and dorsolateral parts of the MGV, respectively, forming narrow bands of terminal axons that extended in the mediolateral direction in the coronal plane of the MGV. The minimum dorsoventral width of the bands ranged approximately from 100 to 300 microm. Besides, the more rostral portion of area Te1 tended to project to the more rostral side of the MGV. The projections to the MGD consistently arborized in its ventral margin made up of the deep dorsal nucleus of the MGD. A similar weak topography along the rostrocaudal direction was observed in the projections to the MGD. Large terminals were occasionally found in the MGD after the injections involving cortical layer V. The distribution of large terminals also appeared topographic along with small terminals that were the major component of labeling. Collaterals of labeled axons produced slabs of terminal field in the thalamic reticular nucleus, which also exhibited a weak topography of distribution. These results provide insights into the structural basis of corticofugal modulations related to the tonotopic organizations in the cortex and MG.     

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     

Efferent connections of "posterodorsal" auditory area in the rat cortex: implications for auditory spatial processing

We examined efferent connections of the cortical auditory field that receives thalamic afferents specifically from the suprageniculate nucleus (SG) and the dorsal division (MGD) of the medial geniculate body (MG) in the rat [Neuroscience 117 (2003) 1003]. The examined cortical region was adjacent to the caudodorsal border (4.8-7.0 mm posterior to bregma) of the primary auditory area (area Te1) and exhibited relatively late auditory response and high best frequency, compared with the caudal end of area Te1. On the basis of the location and auditory response property, the cortical region is considered identical to "posterodorsal" auditory area (PD). Injections of biocytin in PD revealed characteristic projections, which terminated in cortical areas and subcortical structures that play pivotal roles in directed attention and space processing. The most noticeable cortical terminal field appeared as dense plexuses of axons in area Oc2M, the posterior parietal cortex. Small terminal fields were scattered in area frontal cortex, area 2 that comprises the frontal eye field. The subcortical terminal fields were observed in the pontine nucleus, the nucleus of the brachium inferior colliculus, and the intermediate and deep layers of the superior colliculus. Corticostriatal projections targeted two discrete regions of the caudate putamen: the top of the middle part and the caudal end. It is noteworthy that the inferior colliculus and amygdala virtually received no projection. Corticothalamic projections terminated in the MGD, the SG, the ventral zone of the ventral division of the MG, the ventral margin of the lateral posterior nucleus (LP), and the caudodorsal part of the posterior thalamic nuclear group (Po). Large terminals were found in the MGD, SG, LP and Po besides small terminals, the major component of labeling. The results suggest that PD is an auditory area that plays an important role in spatial processing linked to directed attention and motor function. The results extend to the rat findings from nonhuman primates suggesting the existence of a posterodorsal processing stream for auditory spatial perception.     

Thalamic projections to the auditory cortex in the rufous horseshoe bat (<Emphasis Type="Italic">Rhinolophus rouxi)</Emphasis>

In this study, we analyzed the thalamic connections to the parietal or dorsal auditory cortical fields of the horseshoe bat, Rhinolophus rouxi. The data of the present study were collected as part of a combined investigation of physiologic properties, neuroarchitecture, and chemoarchitecture as well as connectivity of cortical fields in Rhinolophus, in order to establish a neuroanatomically and functionally coherent view of the auditory cortex. Horseradish peroxidase or wheat-germ-agglutinated horseradish peroxidase deposits were made into cortical fields after mapping response properties. The dorsal fields of the auditory cortex span nearly the entire parietal region and comprise more than half of the nonprimary auditory cortex. In contrast to the temporal fields of the auditory cortex, which receive input mainly from the ventral medial geniculate body (or “main sensory nucleus”), the dorsal fields of the auditory cortex receive strong input from the “associated nuclei” of the medial geniculate body, especially from the anterior dorsal nucleus of the medial geniculate body. The anterior dorsal nucleus is as significant for the dorsal fields of the auditory cortex as the ventral nucleus of the medial geniculate body is for the temporal fields of the auditory cortex. Additionally, the multisensory nuclei of the medial geniculate body provide a large share of the total input to the nonprimary fields of the auditory cortex. Comparing the organization of thalamic auditory cortical afferents in Rhinolophus with other species demonstrates the strong organizational similarity of this bat’s auditory cortex with that of other mammals, including primates, and provides further evidence that the bat is a relevant and valuable model for studying mammalian auditory function.     

Topographic organization of the auditory thalamocortical system in the albino rat

Summary The organization of the auditory thalamocortical connections was studied in rats. Retrograde transport of horseradish peroxidase conjugated to wheat germ agglutinin following injections into parietal, occipital and temporal cortex was used. The medial geniculate body, the suprageniculate, the lateral part of the nucleus posterior thalami, the posterior part of the nucleus lateralis thalami, and the nucleus ventroposterior project to the investigated part of the neocortex. Corresponding to different patterns of labeling, five areas of auditory neocortex were distinguished: 1. The rostral area is innervated by neurons of the nucleus ventroposterior, the lateral part of the nucleus posterior thalami, and the medial division of the medial geniculate body. 2. The dorsal area is innervated by neurons of the suprageniculate, the posterior part of the nucleus lateralis thalami and the rostral region of the dorsal division of the medial geniculate body. 3. The caudal area is innervated by neurons of the posterior part of the nucleus lateralis thalami, the suprageniculate, the medial division, the caudal region of the dorsal division and the ventrolateral nucleus of the medial geniculate body. 4. The ventral area is innervated by neurons of the suprageniculate, the medial division, the caudal region of the dorsal division, and the ventrolateral nucleus of the medial geniculate body. 5. The core area of the temporal cortex is exclusively connected to the caudal region of the medial division and the ventral division of the medial geniculate body.The findings of the present study indicate topographic organizations of the ventral division of the medial geniculate body and of the corea area. Four segments (a-d) of the ventral division each show a different set of topographic axes. They correspond to sets of topographic axes in the core area of the auditory cortex. These topographies characterize the segments which are each exclusively connected to one of the four fields of the core area.Abbreviations AC Auditory Cortex - c Caudal - d Dorsal - FR Fissura rhinalis, Rhinal Fissure - l Lateral - LTP Nucleus lateralis thalami, pars posterior - m Medial - MGB Medial geniculate body - MGBd Medial geniculate body, dorsal division - MGBm Medial geniculate body, medial division - MGBmc Medial geniculate body, caudal third of MGBm - MGBv Medial geniculate body, ventral division - MGBvl Medial geniculate body, ventrolateral nucleus - NPT Nucleus posterior thalami, pars lateralis - r Rostral - SG Suprageniculatum - VP Nucleus ventroposterior     

Comparison of the fine structure of cortical and collicular terminals in the rat medial geniculate body

Neurons throughout the rat medial geniculate body, including the dorsal and ventral divisions, display a variety of responses to auditory stimuli. To investigate possible structural determinants of this variability, measurements of axon terminal profile area and postsynaptic dendrite diameter were made on inferior colliculus and corticothalamic terminal profiles in the medial geniculate body identified by anterograde tracer labeling following injections into the inferior colliculus or cortex. Over 90% of the synapses observed were axodendritic, with few axosomatic synapses. Small (<0.5 μm²) and large (>1.0 μm²) collicular profiles were found throughout the medial geniculate, but were smaller on average in the dorsal division (0.49±0.49 μm²) than in the ventral division (0.70±0.64 μm²). Almost all corticothalamic profiles were small and ended on small-caliber dendrites (0.57±0.25 μm diameter) throughout the medial geniculate. A few very large (>2.0 μm²) corticothalamic profiles were found in the dorsal division and in the marginal zone of the medial geniculate. GABA immunostaining demonstrated the presence of GABAergic profiles arising from cells in the inferior colliculus. These profiles were compared with GABAergic profiles not labeled with anterograde tracer, which were presumed to be unlabeled inferior colliculus profiles or thalamic reticular nucleus profiles. The distributions of dendritic diameters postsynaptic to collicular, cortical and unlabeled GABAergic profiles were compared with dendritic diameters of intracellularly labeled medial geniculate neurons from rat brain slices.

Our results demonstrate a corticothalamic projection to medial geniculate body that is similar to other sensory corticothalamic projections. However, the heterogeneous distributions of excitatory inferior collicular terminal sizes and postsynaptic dendritic diameters, along with the presence of a GABAergic inferior collicular projection to dendrites in the medial geniculate body, suggest a colliculogeniculate projection that is more complex than the ascending projections to other sensory thalamic nuclei. These findings may be useful in understanding some of the differences in the response characteristics of medial geniculate neurons in vivo.     

Evidence for different patterns of post-translational processing of pro-enkephalin in the bovine adrenal, colon and striatum indicated by radioimmunoassay using region-specific antisera to Met-Enk-Arg6-Phe7 and Met-Enk-Arg6-Gly7-Leu8

Thalamic afferents to layer 1 of the auditory cortex in the cat have been studied using retrograde axonal transport of horseradish peroxidase. The magnocellular part of the medial geniculate nucleus sends fibers to layer 1 of the primary and secondary auditory areas and of the dorsal division of the posterior ectosylvian area. The dorsal principal part and the ventromedial portion of the ventral principal part send only a few fibers to layer 1 of these cortical areas.     

Neocortical connections in fetal cats

The major extrinsic projections to and from visual and auditory areas of cerebral cortex were examined in fetal cats between 46 and 60 days of gestation (E46-E60) using axonal transport of horseradish peroxidase either alone or in combination with tritiated proline. Projections to visual cortex from the dorsal lateral geniculate nucleus and lateral-posterior/pulvinar complex exist by E46, and those from the contralateral hemisphere, claustrum, putamen, and central lateral nucleus of the thalamus are present by E54-E56. In addition, cells in the medial geniculate nucleus project to auditory cortex by E55. At E54-E56 efferent cortical projections reach the contralateral hemisphere, claustrum, putamen, lateral-posterior/pulvinar complex and reticular nucleus of the thalamus. Cells in visual cortex also project to the dorsal and ventral lateral geniculate nuclei, pretectum, superior colliculus and pontine nuclei, and cells in auditory cortex project to the medial geniculate nucleus. Except for interhemispheric projections, all pathways demonstrated are ipsilateral, and projections linking cerebral cortex with claustrum, dorsal lateral geniculate nucleus and lateral-posterior/pulvinar complex are reciprocal. The reciprocal projections formed with the dorsal lateral geniculate nucleus, lateral-posterior/pulvinar complex and the claustrum show a greater degree of topological organization compared to the projections formed with the contralateral hemisphere and superior colliculus, which show little or no topological order. Therefore, the results of the present study show that the major extrinsic projections of the cat's visual and auditory cortical areas with subcortical structures are present by the eighth week of gestation, and that the origins and terminations of many of these projections are arranged topologically.     

Thalamic and temporal cortex input to medial prefrontal cortex in rhesus monkeys

 To determine the source of thalamic input to the medial aspect of the prefrontal cortex, we injected retrograde tracers (wheat germ agglutinin conjugated to horseradish peroxidase, nuclear yellow, and/or bisbenzimide) into seven medial prefrontal sites and anterograde tracers (tritiated amino acids) into six thalamic sites, in a total of nine rhesus monkeys. The results indicated that ventral precallosal and subcallosal areas 14 and 25, and the ventral, subcallosal part of area 32, all receive projections from the mediodorsal portion of the magnocellular division of the medial dorsal nucleus (MDmc). The dorsal, precallosal part of area 32 receives projections mainly from the dorsal portion of the parvocellular division of the medial dorsal nucleus (MDpc), which also provides some input to area 14. Polar area 10 receives input from both MDpc and the densocellular division of the medial dorsal nucleus (MDdc), as does supracallosal area 24. Area 24 receives additional input from the anterior medial nucleus and midline nuclei. All medial prefrontal cortical areas were also found to receive projections from a number of cortical regions within the temporal lobe, such as the temporal pole, superior temporal gyrus, and parahippocampal gyrus. Areas 24, 25, and 32 receive, in addition, input from the entorhinal cortex. Combining these results with prior anatomical and behavioral data, we conclude that medial temporal areas that are important for object recognition memory send information directly both to dorsal medial prefrontal areas 24 and 32 and to ventral medial prefrontal areas 14 and 25. Only the latter two areas have additional access to this information via projections from the mediodorsal part of MDmc. Received: 1 March 1996 / Accepted: 13 January 1997     

Efferent connections of an auditory area in the caudal insular cortex of the rat: anatomical nodes for cortical streams of auditory processing and cross-modal sensory interactions

In the rat cortex, the two non-primary auditory areas, posterodorsal and ventral auditory areas, may constitute the two streams of auditory processing in their distinct projections to the posterior parietal and insular cortices. The posterior parietal cortex is considered crucial for auditory spatial processing and directed attention, while possible auditory function of the insular cortex is largely unclear. In this study, we electrophysiologically delineated an auditory area in the caudal part of the granular insular cortex (insular auditory area, IA) and examined efferent connections of IA with anterograde tracer biocytin to deduce the functional significance of IA. IA projected to the rostral agranular insular cortex, a component of the lateral prefrontal cortex. IA also projected to the adjacent dysgranular insular cortex and the caudal agranular insular cortex and sent feedback projections to cortical layer I of the primary and secondary somatosensory areas. Corticofugal projections terminated in auditory, somatosensory and visceral thalamic nuclei, and the bottom of the thalamic reticular nucleus that could overlap the visceral sector. The ventral part of the caudate putamen, the external cortex of the inferior colliculus and the central amygdaloid nucleus were also the main targets. IA exhibited neural response to transcutaneous electrical stimulation of the forepaw in addition to acoustic stimulation (noise bursts and pure tones). The results suggest that IA subserves diverse functions associated with somatosensory, nociceptive and visceral processing that may underlie sound-driven emotional and autonomic responses. IA, being potentially involved in such extensive cross-modal sensory interactions, could also be an important anatomical node of auditory processing linked to higher neural processing in the prefrontal cortex.     

Overlapping projections to the amygdala and striatum from auditory processing areas of the thalamus and cortex.

The purpose of this study was to advance our understanding of the anatomical organization of sensory projections to the amygdala, and specifically to identify potential interactions within the amygdala between thalamic and cortical sensory projections of a single sensory modality. Thus, interconnections between the amygdala and acoustic processing areas of the thalamus and cortex were examined in the rat using WGA-HRP as an anterograde and a retrograde axonal tracer. Injections placed in medial aspects of the medial geniculate body (MGB) produced anterograde transport to the lateral nucleus of the amygdala and to adjacent areas of the striatum. Injections of primary auditory cortex (TE1) produced no transport to amygdala. In contrast, injections ventral to TE1 involving TE3 and perirhinal periallocortex (PRh) produced anterograde transport in the subcortical forebrain that was indistinguishable from that produced by the MGB injections. The TE3 and PRh injections also resulted in retrograde transport to primary auditory cortex and to MGB, thus confirming the involvement of these ventral cortical areas in auditory functions. Injections of the lateral nucleus of the amygdala resulted in retrograde transport back to the medial areas of MGB and to temporal cortical areas PRh, TE3, and the ventral most part of TE1. Thus, auditory processing regions of the thalamus and cortex give rise to overlapping (possibly convergent) projections to the lateral nucleus of the amygdala. These projections may allow diverse auditory signals to act on common ensembles of amygdaloid neurons and may therefore play a role in the integration of sensory messages leading to emotional reactions.     

Afferent connections of dorsal and ventral agranular insular cortex in the hamsterMesocricetus auratus

The agranular insular cortex is transitional in location and structure between the ventrally adjacent olfactory allocortex primutivus and dorsally adjacent sensory-motor isocortex. Its ventral anterior division receives major afferent projections from olfactory areas of the limbic system (posterior primary olfactory cortex, posterolateral cortical amygdaloid nucleus and lateral entorhinal cortex) while its dorsal anterior division does so from non-olfactory limbic areas (lateral and basolateral amygdaloid nuclei).The medial segment of the mediodorsal thalamic nucleus projects to both the ventral and dorsal divisions of the agranular insular cortex, to the former from its anterior portion and to the latter from its posterior portion. Other thalamic inputs to the two divisions arise from the gelatinosus, central medial, rhomboid and parafascicular nuclei. The dorsal division, but not the ventral division, receives input from neurons in the lateral hypothalamus and posterior hypothalamus.The medial frontal cortex projects topographically and bilaterally upon both ventral and dorsal anterior insular cortex, to the former from the ventrally located medial orbital and infralimbic areas, to the latter from the dorsally-located anterior cingulate and medial precentral areas, and to both from the intermediately located prelimbic area. Similarly, the ipsilateral posterior agranular insular cortex and perirhinal cortex project in a topographic manner upon the two divisions of the agranular insular cortex.Commissural input to both divisions originates from pyramidal neurons in the respective contralateral homotopical cortical area. In each case, pyramidal neurons in layer V contribute 90% of this projection and 10% arises from layer III pyramidals.In the brainstem, the dorsal raphe nucleus projects to the ventral and dorsal divisions of the agranular insular cortex and the parabrachial nucleus projects to the dorsal division.Based on their cytoarchitecture, pattern of afferent connections and known functional properties, we consider the ventral and dorsal divisions of the agranular insular cortex to be, respectively, periallocortical and proisocortical portions of the limbic cortex.     

Connections to the lateral posterior-pulvinar thalamic complex from the reticular and ventral lateral geniculate thalamic nuclei: a topographical study in the cat

The projections from the reticular thalamic nucleus and the ventral lateral geniculate nucleus to the lateral posterior-pulvinar thalamic complex were studied in the adult cat using the retrograde transport of horseradish peroxidase. Small, stereotaxically guided injections of the enzyme were placed in the various nuclei of this complex, including the pulvinar, lateralis intermedius oralis, lateralis intermedius caudalis, lateralis posterior lateralis, lateralis posterior medialis and lateralis medialis nuclei. The distribution of labeled neurons indicates that these nuclei receive topographically organized projections from the reticular and ventral lateral geniculate nuclei. The pulvinar nucleus receives only very scarce projections from the reticular thalamic nucleus originating in its posterodorsal and posteroventral sectors. The reticular projection to the nucleus lateralis intermedius oralis is even sparser. The nuclei lateralis intermedius caudalis, lateralis posterior lateralis and lateralis posterior medialis receive substantial projections from the suprageniculate sector of the reticular thalamic nucleus. The nucleus lateralis medialis receives an abundant projection from the three sectors (suprageniculate, pregeniculate and infrageniculate) of the reticular thalamic nucleus. Except for the lateralis intermedius caudalis, all nuclei of the lateral posterior-pulvinar complex receive consistent projections from the ventral lateral geniculate nucleus, the nucleus lateralis medialis receiving the densest one. Our findings suggest that visual, auditory, somatosensory, motor and limbic impulses from thalamic nuclei and from primary sensory and association cortical areas modulate the activity of the nucleus lateralis medialis via the reticular thalamic nucleus. The remaining nuclei of the lateral posterior-pulvinar complex are mainly modulated by sectors of the reticular thalamic nucleus that receive afferent connections from visual structures. The intrathalamic projections arising from the ventral lateral geniculate nucleus may be the way through which visuomotor inputs reach the different components of the lateral posterior-pulvinar thalamic complex.     

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.     

Multisensory processing via early cortical stages: Connections of the primary auditory cortical field with other sensory systems

It is still a popular view that primary sensory cortices are unimodal, but recent physiological studies have shown that under certain behavioral conditions primary sensory cortices can also be activated by multiple other modalities. Here, we investigate the anatomical substrate, which may underlie multisensory processes at the level of the primary auditory cortex (field AI), and which may, in turn, enable AI to influence other sensory systems. We approached this issue by means of the axonal transport of the sensitive bidirectional neuronal tracer fluorescein-labeled dextran which was injected into AI of Mongolian gerbils (Meriones unguiculatus). Of the total number of retrogradely labeled cell bodies (i.e. cells of origin of direct projections to AI) found in non-auditory sensory and multisensory brain areas, approximately 40% were in cortical areas and 60% in subcortical structures. Of the cell bodies in the cortical areas about 82% were located in multisensory cortex, viz., the dorsoposterior and ventroposterior, posterior parietal cortex, the claustrum, and the endopiriform nucleus, 10% were located in the primary somatosensory cortex (hindlimb and trunk region), and 8% in secondary visual cortex. The cortical regions with retrogradely labeled cells also contained anterogradely labeled axons and their terminations, i.e. they are also target areas of direct projections from AI. In addition, the primary olfactory cortex was identified as a target area of projections from AI. The laminar pattern of corticocortical connections suggests that AI receives primarily cortical feedback-type inputs and projects in a feedforward manner to its target areas. Of the labeled cell bodies in the subcortical structures, approximately 90% were located in multisensory thalamic, 4% in visual thalamic, and 6% in multisensory lower brainstem structures. At subcortical levels, we observed a similar correspondence of retrogradely labeled cells and anterogradely labeled axons and terminals in visual (posterior limitans thalamic nucleus) and multisensory thalamic nuclei (dorsal and medial division of the medial geniculate body, suprageniculate nucleus, posterior thalamic cell group, zona incerta), and in the multisensory nucleus of the brachium of the inferior colliculus. Retrograde, but not anterograde, labeling was found in the multisensory pontine reticular formation, particularly in the reticulotegmental nucleus of the pons. Conversely, anterograde, but no retrograde, labeling was found in the visual laterodorsal and lateroposterior thalamic nuclei, in the multisensory peripeduncular, posterior intralaminar, and reticular thalamic nuclei, as well as in the multisensory superior and pericentral inferior colliculi (including cuneiform and sagulum nucleus), pontine nuclei, and periaqueductal gray. Our study supports the notion that AI is not merely involved in the analysis of auditory stimulus properties but also in processing of other sensory and multisensory information. Since AI is directly connected to other primary sensory cortices (viz. the somatosensory and olfactory ones) multisensory information is probably also processed in these cortices. This suggests more generally, that primary sensory cortices may not be unimodal.