Responsiveness of cells in the cat's superior colliculus to textured visual stimuli

Summary Responses to texture motion (visual noise) were investigated in the superior colliculus of paralysed cats, lightly anaesthetized with N₂O/O₂ supplemented with pentobarbitone or Althesin. Within the superficial layers two classes of texture-sensitive neurones were found: Type I units with weak responses to noise, often related to specific elements in the texture and Type II units which were driven independently of the texture structure, and tended to be recorded deep to the Type I units. Type III units recorded from the deep collicular layers were insensitive to texture. Anatomical bases for this differential sensitivity and the notion of two collicular subsystems are discussed.     

Differential responsiveness of simple and complex cells in cat striate cortex to visual texture

Summary The responsiveness of 254 simple and complex striate cortical cells to various forms of static and dynamic textured visual stimuli was studied in cats, lightly anaesthetised with N₂O/O₂ mixtures supplemented with pentobarbitone.Simple cells were unresponsive to all forms of visual noise presented alone, although about 70% showed a change in responsiveness to conventional bar stimuli when these were presented on moving, rather than stationary, static-noise backgrounds. Bar responses were depressed by background texture motion in a majority of cells (54%), but were actually enhanced in a few instances (16%).In contrast, all complex cells were to some extent responsive to bars of static visual noise moving over stationary backgrounds of similar texture, or to motion of a whole field of static noise. The optimal velocity for noise was generally lower than for bar stimuli.Since moving noise backgrounds were excitatory for complex cells, they tended to reduce specific responses to bar stimulation; in addition, directional bias could be modified by direction and velocity of background motion.Complex cells fell into two overlapping groups as regards their relative sensitivity to light or dark bars and visual noise. Extreme examples were insensitive to conventional bar or edge stimuli while responding briskly to moving noise.In many complex cells, the preferred directions for motion of noise and of an optimally oriented black/white bar were dissimilar.The ocular dominance and the degree of binocular facilitation of some complex cells differed for bar stimuli and visual texture.Preliminary evidence suggests that the deep-layer complex cells (those tolerant of misalignment of line elements; Hammond and MacKay, 1976) were most sensitive to visual noise. Superficial-layer complex cells (those preferring alignment) were less responsive to noise.Only complex-type hypercomplex cells showed any response to visual noise.We conclude that, since simple cells are unresponsive to noise, they cannot provide the sole input to complex cells. The differences in the response of some complex cells to rectilinear and textured stimuli throw a new light on their rôle in cortical information-processing. In particular, it tells against the hypothesis that they act as a second stage in the abstraction of edge-orientation.     

GABA-receptor activation in the globus pallidus and entopeduncular nucleus: opposite effects on reaction time performance in the cat

The possible role of GABAergic mechanisms in the control of the basal ganglia output structures, the globus pallidus (GP) and the entopeduncular nucleus (EP), was studied in cats performing a conditioned flexion movement triggered by an auditory stimulus. The effects of discrete unilateral microinjections of low doses of the GABA_A receptor agonist (muscimol 5–100 ng/ 0.5 l) and antagonist (bicuculline methiodide 25–150 ng/0.5 l) in the GP and the EP were tested on the motor performance of eight animals trained to release a lever in a simple reaction time (RT) schedule after an auditory stimulus. Control injections in neighboring structures did not induce any effect except with five- to tenfold higher doses in the closest injection sites. The dose of 20 ng muscimol injected into the ventral and medial part of the GP produced an arrest of the performance after a few unsuccessful trials (over the RT reinforcement limit of 500 ms), while muscimol injected in sites located in the lateral GP resulted in a dose-dependent lengthening in RTs, with a concomitant increase in the force change latency. In most of the subjects, the force exerted on the lever was higher after muscimol than after vehicle injection. Force change velocity was then significantly increased. In contrast, muscimol injected in the ventral and rostral region of the EP produced a decrease in RTs or a complete cessation of responding after a high number of anticipatory responses (release of the lever before the trigger stimulus). No significant changes in the force change latency could be observed while there was a non-significant tendency for the force levels to be lowered. Bicuculline injections in the EP were found to increase RTs with a concomitant increase in force change latency and a slowness of velocity, while no significant effect was observed following injections in the GP. These results suggest that a balance between GABAergic activity in the two output nuclei of the basal ganglia, the GP and the EP, is crucial for the correct initiation and execution of the conditioned motor task.     

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     

Properties and localization of the anterior semicircular canal-activated vestibulocollic neurons in the cat

Summary Unit activites of secondary vestibular neurons that selectively responded to stimulation of the anterior semicircular canal nerve (ACN) were recorded extracellularly in the anesthetized cat. Axonal pathways and projections in the spinal cord of the ACN-activated neurons were examined by recording their antidromic responses to stimulation of the lateral and medial vestibulospinal tracts (LVST and MVST), and the bilateral neck extensor motoneuron pools in the C₁segment (C₁dorsal rami [DR] motoneuron pools). In order to determine whether the neurons had ascending axon collaterals to the extraocular motoneurons, the contralateral (c-) inferior oblique (IO) motoneuron pool was also stimulated. Twenty-seven neurons sent their axons to the ipsilateral (i-) C₁DR motoneuron pool via the LVST without any projection to the extraocular motoneuron pool. All the cells except one were located in the ventral part of the lateral vestibular nucleus. This pathway produced monosynaptic EPSPs with short time-to-peak and short half-width in C₁DR motoneurons (16/16 motoneurons). Eight neurons sent axons to the i-C₁DR motoneuron pool via the MVST without any to the extraocular motoneuron pool. Cell somata were located in the descending nucleus or in the ventral part of the lateral nucleus. These neurons did not produce postsynaptic potentials (PSPs) in any C₁DR motoneurons. All thirty-five neurons sending axons to the c-C₁DR motoneuron pool have ascending axon collaterals to the c-IO motoneuron pool.     

Convergence of skin reflex and corticospinal effects in segmental and propriospinal pathways to forelimb motoneurones in the cat

The organization of facilitatory convergence from cutaneous afferents (Skin) and the corticospinal tract (pyramidal tract, Pyr) in pathways to forelimb motoneurones of mainly distal muscles was studied in anaesthetized cats by analysing postsynaptic potentials (PSPs), which were spatially facilitated by combinations of stimuli to the two sources at different time intervals. Conditioning Pyr volleys facilitated Skin-evoked PSPs of fixed (1.2–3.6 ms) central latencies (Skin PSPs), suggesting that disynaptic and polysynaptic skin reflex pathways are facilitated from the pyramidal tract. The shortest latencies (1.2–1.7 ms) of pyramidal facilitation suggested direct connection of pyramidal fibres with last order neurones of skin reflex pathways. Conditioning Skin volleys facilitated Pyr-evoked PSPs of fixed, mostly disynaptic latencies (1.0–2.5 ms; Pyr PSPs), suggesting that pyramido-motoneuronal pathways are facilitated from Skin at a premotoneuronal level. The shortest pathway from skin afferents to the premotor neurones appeared to be monosynaptic. Although Pyr and Skin volleys were mutually facilitating, the facilitation curve of Pyr PSPs and that of Skin PSPs were discontinuous to each other, with the peak facilitation at different Skin-Pyr volley intervals. Transection of the dorsal column (DC) at the C5/C6 border had little effect on the latencies or amplitudes evoked by maximal stimulation and the pyramidal facilitation of Skin PSPs. In contrast, the facilitation of Pyr PSPs by Skin stimulation was greatly decreased after the DC transection, and the facilitation curve of Pyr PSPs was continuous to that of Skin PSPs, with no separate peak. Latencies of Pyr PSPs ranged similarly to those in DC intact preparations. More rostral DC transection (C4/C5 border) reduced Skin-facilitated Pyr excitatory PSPs (EPSPs) less than C5/C6 lesions, suggesting that the C5 segment also contains neurones mediating Skin-facilitated Pyr EPSPs. The results show that convergence from skin afferents and the corticospinal tract occurs at premotor pathways of different cervical segments. We suggest that corticospinal facilitation of skin reflex occurs mostly in the brachial segments and Skin facilitation of cortico-motoneuronal effects takes place largely in the rostral cervical segments and partly in the brachial segments.     

Changes in extracellular potassium concentration in cat spinal cord in response to innocuous and noxious stimulation of legs with healthy and inflamed knee joints

Summary In 20 cats anaesthetized with alpha-chloralose and spinalized at the thoracolumbar junction we investigated the role of stimulation induced accumulation of extracellular potassium in the spinal cord in the processing of nociceptive discharges from the knee joint. For that we electrically stimulated the posterior articular nerve of the knee. We further performed innocuous and noxious stimulation of the knee and of other parts of the leg and studied the effect of an acute inflammation of the knee on [K⁺]₀ in the spinal cord. Innocuous stimulation of the skin (brushing or touching) and innocuous movements in the knee joint all induced rises in [K⁺]₀ which were maximal at recording depths of 1500 to 2200 m below the surface of the cord dorsum. Peak increases were 0.4 mM for touching the leg and 1.7 mM during rhythmic flexion/ extension of the knee joint. Noxious stimulation of the skin, the paw, the tendon and noxious movements of the knee joint also produced rises in [K⁺]₀, which were somewhat larger for the individual types of stimuli than those produced by innocuous intensities. Electrical stimulation of the posterior articular nerve induced rises in [K⁺]₀ by up to 0.6 mM. Stimulus intensities sufficient to activate unmyelinated group IV fibers were only slightly effective in raising [K⁺]₀ above the levels reached during stimulation of myelinated group II and III fibers. During development of an acute inflammation of the knee joint (induced by kaolin and carrageenan), increases in [K⁺]₀ and associated field potentials became larger by about 25%. We assume that this reflects an increase in neuronal responses. In conclusion, changes in [K⁺]₀ in the spinal cord are some-what larger during noxious stimulation than during innocuous stimulation. The absolute level reached depended more on the site and type of stimulation than on the actual stimulus intensity itself. Hence a critical role of spinal K⁺ accumulation for nociception is unlikely.     

Stimulation of cranial vessels excites nociceptive neurones in several thalamic nuclei of the cat

Summary Extracellular recordings were made in the thalamus of cats anaesthetized with chloralose and urethane following electrical, mechanical and chemical stimulation of the superior sagittal sinus or middle meningeal artery. Facial receptive fields were looked for using electrical and mechanical stimuli. The locations of fifty-six cells were verified histologically. Twenty six cells were located in the ventroposteromedial nucleus (VPM) and six in its ventral periphery (VPMvp). All units in VPM had facial receptive fields, usually involving the first trigeminal division. Cells with nociceptive receptive fields or responding to the craniovascular application of bradykinin were often found in the periphery or “shell” region of VPM. Other craniovascular nociceptive cells were found in VPMvp, in the posterior group and in the intralaminar complex. This study shows that craniovascular afferents in the cat project to several thalamic nuclei and implicate VPM especially in craniovascular nociception.     

Synaptic mechanisms acting on lumbar motoneurons during postural augmentation induced by serotonin injection into the rostral pontine reticular formation in decerebrate cats

Intrapontine microinjections of serotonin in acutely decerebrated cats resulted in the bilateral augmentation of the postural muscle tone of the hindlimbs. Optimal injection sites were located in the dorsomedial part of the rostral pontine reticular formation corresponding to the nucleus reticularis ponds oralis (NRPo). In this study, attempts were made to elucidate the cellular basis for the serotoninergically induced augmentation of postural muscle tone by recording the electromyographic (EMG) activity of hindlimb extensor muscles, the monosynaptic reflex responses evoked by electrical stimulation of group Ia muscle afferent fibres and the membrane potentials of hindlimb alpha-motoneurons (MNs). Serotonin injections resulted not only in the augmentation of the EMG activity of gastrocnemius soleus muscles, but also in the restoration of EMG suppression, which was induced by previous injection of carbachol into the NRPo. Extensor and flexor monosynaptic reflex responses were facilitated by serotonin injections into the NRPo. Such reflex facilitation was not induced by serotonin injections into the mesencephalic or the medullary reticular formation. Intrapontine serotonin injections resulted in membrane depolarization of extensor and flexor MNs with decreases in input resistance and rheobase. Spontaneous depolarizing synaptic potentials (EPSPs) increased in both frequency and amplitude. Peak voltage of Ia monosynaptic EPSPs also increased. Serotonin injections which followed carbachol injections resulted in membrane depolarization of MNs along with an increase in the frequency of spontaneous EPSPs and a decrease in carbachol-induced inhibitory postsynaptic potentials. Following pontine carbachol injections, antidromic and orthodromic responses in MNs were suppressed. Discharges of MNs evoked by intracellular current injections were also suppressed, but were restored following serotonin injections. These results indicate that postsynaptic excitation, presynaptic facilitation and disinhibition (withdrawal of postsynaptic inhibition) simultaneously act on the hindlimb MNs during serotonin-induced postural augmentation and restoration.     

Alterations in short-term retention, conditioned avoidance response acquisition and motivation following aluminum induced neurofibrillary degeneration

Aluminum chloride induced neurofibrillary degeneration may provide a useful model for the study of a human dementia process. This possibility was assessed in cats trained to perform on a delayed-response task, a conditioned avoidance task, visual and temporal discrimination tasks and a motivational task involving rewarding intracranial electrical stimulation. After an initial asymptomatic period short term retention and acquisition of a conditioned avoidance response were selectively impaired. The associated ultrastructural abnormalities plausibly implicate the cytoplasmic streaming mechanism in the cellular substrate for some retention and acquisition phenomena.