Efferent neurons and suspected interneurons in binocular visual cortex of the awake rabbit: receptive fields and binocular properties

1. In fully awake rabbits the stability of the two eyes was monitored and was sufficient to enable receptive-field analysis of antidromically identified efferent neurons and suspected interneurons in the binocular segment of visual area 1. Efferent neurons analyzed included callosal efferent neurons (CC neurons, n = 52), neurons projecting to visual area 2 (CV2 neurons, n = 35), corticotectal neurons (CT neurons, n = 43), and corticogeniculate neurons (CG neurons, n = 51). Six additional neurons projected a branching axon to both the corpus callosum and visual area 2. 2. Most CC and CV2 neurons were found in layer 2-3 and had receptive fields of the simple type. Only two corticocortical neurons with complex receptive fields were found. Orientation tuning ranges of CC and CV2 simple cells were similar and end stopping was prevalent in both CC (62%) and CV2 (45%) neurons. Axonal conduction velocities of CC and CV2 neurons were low (mean = 3.5 and 1.4 m/s, respectively) and visually nonresponsive CC neurons (19%) had conduction velocities that were significantly lower than visually responsive neurons. Spontaneous firing rates of corticocortical neurons were low (mean less than 1 spike/s) and these neurons responded to a lower range of stimulus velocities than did corticofugal neurons. 3. Most CG neurons had simple receptive fields and none had a complex field. Orientation tuning ranges of these neurons were comparable to those of CC and CV2 neurons, but a significantly smaller proportion (12%) were end stopped. Both spontaneous firing rates (mean = less than 1 spike/s) and axonal conduction velocities (mean = 2.4 m/s) of CG neurons were low and, as was found for CC neurons, visually nonresponsive CG neurons (25%) had significantly lower conduction velocities than did visually responsive neurons. 4. CT neurons had receptive fields that were predominantly complex (37%), motion/uniform (28%), or simple (26%). Conduction velocities (mean = 10.9 m/s) and spontaneous firing rates (mean = 7 spikes/s) of CT neurons of all receptive-field types were much higher than those of CC, CV2, and CG neurons. 5. An additional class of neurons was studied that responded synaptically at a short latency to electrical stimulation of the dorsal lateral geniculate nucleus (LGNd) with a burst of three or more spikes at frequencies of 600-900 Hz. These neurons showed a high degree of synaptic convergence, also responding synaptically with a high-frequency burst of spikes to stimulation of both visual area 2 and the corpus callosum.(ABSTRACT TRUNCATED AT 400 WORDS)     

Receptive-field and axonal properties of neurons in the dorsal lateral geniculate nucleus of awake unparalyzed rabbits

The intrinsic stability of the rabbit eye was exploited to enable receptive-field analysis of LGNd neurons and optic tract axons in the awake, unparalyzed state. We found eye position to remain within a range of less than 1.0 degrees for periods of 4-5 min, and in some cases for periods in excess of 10 min. Such stability is comparable to that seen in awake monkeys that have been trained to fixate. Receptive fields of dorsal lateral geniculate nucleus (LGNd) neurons were analyzed, and approximately 84% were concentrically organized. This is a higher value than previously reported in this species. In addition, the receptive-field centers of concentric cells were much smaller than those previously reported (mean diameter = 2.5 degrees). Most remaining neurons in the LGNd were either directionally selective (6.5%) or motion/uniform (6.5%). Concentric cells were classified as sustained or transient based on response duration to standing contrast. In the LGNd the receptive fields of sustained concentric cells were predominantly near the horizontal meridian, within the representation of the visual streak, while the receptive-field positions of transient concentric cells were more prevalent in the upper visual field. In the optic tract the receptive-field positions of both sustained and transient cells were more evenly distributed than was seen in the LGNd. Sustained and transient concentric cells in LGNd showed primarily nonlinear spatial summation. The receptive-field properties of LGNd neurons were related to geniculocortical antidromic latency. Most LGNd neurons of all receptive-field classes projected axons to the visual cortex. Thus, any intrinsic interneurons in the rabbit LGNd may have receptive-field properties similar to those of some principal neurons. There was significant overlap in the distribution of antidromic latencies in neurons of different receptive-field classes. Concentric sustained neurons, however, did conduct somewhat more slowly than did concentric transient neurons. Nonvisual sensory stimuli that resulted in EEG arousal (hippocampal theta activity) had a profound effect on the response duration of most (28/32) sustained concentric neurons. For these cells, the sustained response to standing contrast began to diminish and sometimes disappeared after 2-15 s. However, arousing stimuli that resulted in hippocampal theta activity reestablished the sustained response. Such arousing stimuli usually had little or no effect on the discharge of the cell in the absence of visual stimuli. Arousing stimuli had no effect on optic tract axons with sustained concentric receptive-field properties.(ABSTRACT TRUNCATED AT 400 WORDS)     

Receptive-field properties of neurons in different laminae of visual cortex of the cat

1. Receptive-field properties of neurons in the different layers of the visual cortex of normal adult cats were analyzed quantitatively. Neurons were classified into one of two groups: 1) S-cells, which have discrete on- and/or off-regions in their receptive fields and possess inhibitory side bands; 2) C-cells, which do not have discrete on- and off-regions in their receptive fields but display an on-off response to flashing stimuli. Neurons of this type rarely display side-band inhibition. 2. As a group, S-cells display lower relative degrees of binocularity and are more selective for stimulus orientation than C-cells. In addition, within a given lamina the S-cells have smaller receptive fields, lower cutoff velocities, lower peak responses to visual stimulation, and lower spontaneous activity than do the C-cells. 3. S-cells in all layers of the cortex display similar orientation sensitivities, mean spontaneous discharge rates, peak response to visual stimulation, and degrees of binocularity. 4. Many of the receptive-field properties of cortical cells vary with laminar location. Receptive-field sizes and cutoff velocities of S-cells and of C-cells are greater in layers V and VI than in layers II-IV. For S-cells, preferred velocities are also greater in layers V and VI than in layers II-IV. Furthermore, C-cells in layers V and VI display high mean spontaneous discharge rates, weak orientation preferences, high relative degrees of binocularity, and higher peak responses to visual stimulation when compared to C-cells in layers II and III. 5. The receptive-field properties of cells in layers V-VI of the striate cortex suggest that most neurons that have their somata in these laminae receive afferents from LGNd Y-cells. Hence, our results suggest that afferents from LGNd Y-cells may play a major part in the cortical control of subcortical visual functions.     

Efferent neurons and suspected interneurons in S-1 forelimb representation of the awake rabbit: receptive fields and axonal properties

1. Receptive-field properties of antidromically identified efferent neurons within the cutaneous forelimb representation of primary somatosensory cortex (S-1) were examined in fully awake rabbits. Efferent neurons studied included callosal neurons (CC neurons, n = 52), ipsilateral corticocortical neurons (C-IC neurons, n = 48) that project to or beyond the second somatosensory cortical area (S-2), and corticofugal neurons of layer 5 (CF-5 neurons, n = 97) and layer 6 (CF-6 neurons, n = 59) that project to and/or beyond the thalamus. 2. An additional class of neurons was studied that was not activated antidromically from any stimulus site, but which responded synaptically to electrical stimulation of the ventrobasal (VB) thalamus with a burst of three or more spikes at frequencies of 600 to greater than 900 Hz. Most of these neurons also responded synaptically to stimulation of S-2 and the corpus callosum. The action potentials of these neurons were much shorter (mean = 0.45 ms) than those of efferent neurons (mean = 0.95 ms). Such properties have been associated with interneurons found throughout the central nervous system, and these neurons are thereby referred to as suspected interneurons (SINs). 3. CF-5 neurons differed from CC, C-IC, and CF-6 neurons in their spontaneous firing rates, axonal properties, and receptive-field properties. Whereas CF-5 neurons had a mean spontaneous firing rate of 5.5 spikes/s, CC, C-IC, and CF-6 neurons had mean values of less than 1/s. Axonal conduction velocities of CF-5 neurons were much higher (mean = 12.92 m/s) than either CC (mean = 2.15 m/s), C-IC (mean = 1.31 m/s), or CF-6 (mean = 2.53 m/s) neurons. A decrease in antidromic latency (the "supernormal" period) that was dependent on prior impulse activity was seen in the great majority of CC, C-IC, and CF-6 neurons but was either minimal or absent in CF-5 neurons of comparable conduction velocity. A higher proportion of CF-5 neurons (98%) responded to peripheral sensory stimulation than did either CC (75%), C-IC (71%), or CF-6 (51%) neurons. CF-6 and C-IC neurons that did not respond to sensory stimulation had significantly lower axonal conduction velocities and spontaneous firing rates than those that responded to such stimulation. 4. Cutaneous receptive fields were seen in most neurons that could be driven by peripheral stimulation.(ABSTRACT TRUNCATED AT 400 WORDS)     

Efferent neurons and suspected interneurons in second somatosensory cortex of the awake rabbit: receptive fields and axonal properties.

1. Receptive-field properties of antidromically identified efferent neurons within the representation of vibrissae and sinus hairs above the mouth were examined in secondary somatosensory cortex (S-2) of fully awake adult rabbits. Efferent neurons studied included callosal neurons (CC neurons, n = 88), ipsilateral corticocortical neurons (C-IC neurons, n = 51) that project to primary somatosensory cortex (S-1), and corticofugal neurons of layer 5 (CF-5 neurons, n = 63) and layer 6 (CF-6 neurons, n = 42) that project to and/or beyond the thalamus. Appropriate collision tests demonstrated that substantial numbers of corticocortical efferent neurons (21 of 113 tested) project an axon to both the corpus callosum and to ipsilateral S-1. 2. Suspected interneurons (SINs, n = 62) were also studied. These neurons were not activated antidromically from any stimulus site but did respond synaptically to electrical stimulation of the ventrobasal (VB) thalamus with a burst of three or more spikes at frequencies of 600 to greater than 900 Hz. Most of these neurons also responded synaptically to stimulation of S-1 and the corpus callosum. The action potentials of these neurons were much shorter (mean, 0.49 ms) than those of efferent neurons (mean, 1.01 ms). 3. CF-5 neurons differed from CC, C-IC, and CF-6 neurons in their spontaneous firing rates, axonal properties, and receptive-field properties. Whereas CF-5 neurons had a mean spontaneous firing rate of 5.7 spikes/s, CC, C-IC, and CF-6 neurons all had mean values of less than 1/s. Axonal conduction velocities of CF-5 neurons were much higher (mean, 11.90 m/s) than either CC (mean, 2.63 m/s), C-IC (mean, 0.86 m/s), or CF-6 (mean, 1.73 m/s) neurons. A decrease in antidromic latency (the "supernormal" period), which was dependent on prior impulse activity, was seen in most CC, C-IC, and CF-6 neurons but was minimal or absent in CF-5 neurons of comparable conduction velocity. Although all CF-5 neurons responded to peripheral sensory stimulation, many CC (52%), C-IC (49%), and CF-6 (55%) neurons did not. CC and CF-6 neurons that did not respond to sensory stimulation had significantly lower axonal conduction velocities and spontaneous firing rates than those that responded to such stimulation. Whereas no CC, C-IC, or CF-6 neuron responded synaptically to callosal stimulation, 43% of CF-5 neurons (and 78% of SINs) did so respond. Similar differences in synaptic responsivity to stimulation of S-1 were seen in these populations.(ABSTRACT TRUNCATED AT 400 WORDS)     

Response properties of visual cortical neurons in cats reared in stroboscopic illumination

1. The response properties of 182 units were studied in the primary visual cortices (155 in area 18 and 27 in area 17) in eight cats reared from birth in a stroboscopically illuminated environment (frequency, 2/s; duration, 200 microseconds). Multihistogram quantitative testing was carried out in 82 units (64 in area 18 and 18 in area 17). Two hundred three neurons recorded and quantitatively tested in areas 17 and 18 of the normal adult cat were used for comparison. 2. Spatial characteristics of receptive fields investigated using hand-held stimuli were found to be abnormal. The correlation between receptive-field width and eccentricity was lost in area 18 and consequently, receptive fields were significantly wider in area 18 subserving central vision. Cells could be classified according to the spatial characteristics of their receptive fields. There was a much smaller proportion of end-stopped cells in strobe-reared animals. Orientation tuning in the deprived animals was normal except for a small number of cells that showed no selectivity for stimulus orientation. 3. Compilation of velocity-response curves made it possible to classify areas 17 and 18 neurons into four categories: velocity low-pass, velocity broad-band, velocity tuned, and velocity high-pass cells. The proportion of velocity high-pass cells was reduced in area 18 subserving peripheral vision, as was the proportion of velocity-tuned cells in area 18 subserving central vision. 4. In the strobe-reared animal velocity sensitivity was somewhat different from that of the normal animal. Neurons in area 18 subserving the peripheral visual field failed to respond to fast velocities. Neurons in area 17 subserving the central visual field in strobe-reared animals responded to slightly higher velocities than in the normal animal. 5. In the deprived animals the number of neurons that were selective to the direction of motion was strongly reduced. The majority of neurons failed to show a selectivity for direction at all velocities. A number of neurons could be directional at some velocities but were unreliable, since they inverted their preferred direction with velocity changes. 6. Binocular convergence onto visual cortical cells was perturbed. In area 18 the majority of neurons were driven by the contralateral eye. In area 17 most neurons could be driven only by either the ipsilateral or contralateral eye. 7. Quantitative testing (of direction selectivity, sensitivity to high velocities, response latency, and strength) and qualitative testing (receptive-field width, end stopping, and ocular dominance) showed that the normal influence of eccentricity on functional properties was strongly reduced by strobe rearing.     

Physiological properties of primary sensory neurons appropriately and inappropriately innervating skin in the adult rat.

1. We have studied the physiology of sensory neurons innervating skin of the rat hindlimb, in three groups of animals: 1) normal animals; 2) animals in which the sural nerve (Sn) had regenerated to its original cutaneous target; and 3) animals in which the gastrocnemius muscle nerve (Gn) had previously been cut and cross anastomosed with the distal stump of the cut Sn so that its axons regenerated to a foreign target, skin. 2. Single-unit recordings were made from 222 afferents in normal, intact animals. They had conduction velocities of 0.5-53.1 m/s. The conduction velocity distribution had distinct peaks at approximately 37.5, 2.5, and 1.25 m/s, presumably corresponding to A alpha beta-, A delta-, and C-fiber populations. Eighty-two percent of the characterized myelinated fibers had low-threshold mechanosensitive receptive fields, whereas 16% were high threshold, and only 2% appeared to have no receptive field. The very large majority of low-threshold mechanosensitive receptive fields (87%) were rapidly adapting hair follicle afferents. 3. In animals with regenerated Sn, 308 afferents were recorded with conduction velocities of 0.4-58.8 m/s. However, the mean conduction velocity was lower than in control animals (P less than 0.05), and only one peak, at 27.5 m/s, was apparent for myelinated fibers. Eighty-six percent of myelinated fibers were low-threshold mechanosensitive afferents, 8.5% were high-threshold mechanoreceptors (HTMRs), and 5.5% appeared to have no receptive fields. Fewer low-threshold mechanoreceptors (LTMRs; compared with controls) were activated by hair movement (63 vs. 87%). Most of the remainder appeared to be field receptors (which were therefore more commonly observed here than in normal animals). 4. In animals in which the Gn had regenerated to skin, 430 afferents were recorded. These had conduction velocities ranging from 0.6 to 71.4 m/s, and again only one peak was apparent in the myelinated conduction velocity histogram, at approximately 17.5 m/s. Of the myelinated fibers, 79% had low-threshold mechanosensitive receptive fields in skin and 10% high-threshold mechanosensitive receptive fields. The remaining 11% apparently had no receptive field (cf. 5.5% in regenerated Sn). In contrast to normal or regrown sural afferents, only 58% of low-threshold gastrocnemius afferents in skin were rapidly adapting. Of the 42% slowly adapting afferents, many surprisingly responded to hair movement. Thus some gastrocnemius afferents seemed to have retained the adaptation properties characteristic of muscle afferents. Also surprisingly, given that the Gn contains fewer fibers than the Sn, receptive-field areas were not significantly different from regrown or normal sural fibers.(ABSTRACT TRUNCATED AT 400 WORDS)     

Receptive fields and response properties of neurons in layer 4 of ferret visual cortex

The ferret has become a model animal for studies exploring the development of the visual system. However, little is known about the receptive-field structure and response properties of neurons in the adult visual cortex of the ferret. We performed single-unit recordings from neurons in layer 4 of adult ferret primary visual cortex to determine the receptive-field structure and visual-response properties of individual neurons. In particular, we asked what is the spatiotemporal structure of receptive fields of layer 4 neurons and what is the orientation selectivity of layer 4 neurons? Receptive fields of layer 4 neurons were mapped using a white-noise stimulus; orientation selectivity was determined using drifting, sine-wave gratings. Our results show that most neurons (84%) within layer 4 are simple cells with elongated, spatially segregated, ON and OFF subregions. These neurons are also selective for stimulus orientation; peaks in orientation-tuning curves have, on average, a half-width at half-maximum response of 21.5 +/- 1.2 degrees (mean +/- SD). The remaining neurons in layer 4 (16%) lack orientation selectivity and have center/surround receptive fields. Although the organization of geniculate inputs to layer 4 differs substantially between ferret and cat, our results demonstrate that, like in the cat, most neurons in ferret layer 4 are orientation-selective simple cells.     

Receptive-field properties of neurons in binocular and monocular segments of striate cortex in cats raised with binocular lid suture

1. We studied the receptive fields of 171 striate cortical neurons from 17 cats raised with binocular lid suture. Of these, 102 fields were within 10 degrees of the area centralis and the remaining 69 were at least 38 degrees from the vertical meridian. 2. Based on their different response properties, cells were divided into three broad groups: the mappable cells (49%) had clearly defined receptive fields, the unmappable cells (31%) were activated by visual stimuli but had diffuse fields which could not be hand plotted, and the visually inexcitable cells (20%) could not be activated by visual stimuli. Very few (less than or equal to 12% of the total sample) normal simple or complex cells could be found. 3. Orientation selectivity was assessed in these cells. Only 12% displayed orientation selectivity within normal bounds, and these were all mappable cells. None of the unmappable cells had discernible orientation selectivity. 4. Ocular dominance was assessed for 62 of the centrally located receptive fields. Among mappable cells, there was an abnormally low proportion of binocular fields, while no such abnormality was seen for unmappable cells. 5. For 47 of the neurons, average response histograms were compiled for moving stimuli of various parameters in an effort to evoke the maximum discharge or peak response. This peak response was normal for mappable cells but reduced for unmappable cells. 6. We devised a technique for studying potential inhibitory receptive-field zones in these neurons, validated the method in normal striate cortex, and used it to test 20 mappable cells in the lid-sutured cats. None showed the pattern of strong inhibitory side bands seen in normal simple cells, although six showed weak or abnormal inhibitory zones. Interestingly, six of the seven visually inexcitable cells tested by this method had purely inhibitory receptive fields. 7. The effects of binocular suture were essentially identical for the binocular and monocular segments since the cell types and their response properties did not differ between these two areas of cortex. Furthermore, the cortical monocular segments of these cats seemed qualitatively different from the deprived cortical monocular segment after monocular suture. This extends an analogous difference for these cats reported for the monocular segments of the lateral geniculate nucleus. We thus conclude that monocularly and binocularly sutured cats develop by qualitatively different mechanisms. For the former, competition between central synapses related to each eye is a prominent feature of geniculocortical development, whereas, for the latter, such specific forms of geniculocortical development may not obtain.     

Receptive-field properties of neurons in middle temporal visual area (MT) of owl monkeys

Response properties of single neurons in the middle temporal visual area (MT) of anesthetized owl monkeys were determined and quantified for flashed and moving bars of light under computer control for position, orientation, direction of movement, and speed. Receptive-field sizes, ranging from 4 to 25 degrees in width, were considerably larger than receptive fields with corresponding eccentricities in the striate cortex. Neurons were highly binocular with most cells equally or nearly equally activated by either eye. Neurons varied in selectivity for axis and direction of moving bars. Some neurons demonstrated little or no selectivity, others were bidirectional on a single axis, while the largest group was highly selective for direction with little or no response to bar movement opposite to the preferred direction. Over 70% of neurons were classified as highly selective and 90% showed some preference for direction and/or axis of stimulus movement. Neurons typically responded to bar movement only over a restricted range of velocities. The majority of neurons responded best to a particular velocity within the 5-60 degrees/s range, with marked attenuation of the response for velocities greater or less than the preferred. Some neurons failed to show significant response attenuation even at the lowest tested velocity, while other neurons preferred velocities of 100 degrees/s or more and failed to attenuate to the highest velocities. Response magnitude varied with stimulus dimensions. Increasing the length of the moving bar typically increased the magnitude of the response slightly until the stimulus exceeded the receptive-field borders. Other neurons responded less to increases in bar length within the excitatory receptive field. Neurons preferred narrow bars less than 1 degree in width, and marked reductions in responses characteristically occurred with wider stimuli. Moving patterns of randomly placed small dots were often as effective as or more effective than single bars in activating neurons. Selectivity for direction of movement remained for the dot pattern. for the dot pattern. Poststimulus time (PST) histograms of responses to bars flashed at a series of 21 different positions across the receptive field, in the "response-plane" format, indicated a spatially and temporally homogeneous receptive-field structure for nearly all neurons. Cells characteristically showed transient excitation at both stimulus onset and offset for all effective stimulus locations. Some cells responded mainly at bright stimulus onset or offset.     

Interrelations of the rat's thalamic reticular and dorsal lateral geniculate nuclei

Summary Electrophysiological and neuroanatomical techniques have been used to study the properties of cells in the reticular nucleus of the thalamus (RNT) responsive to photic stimuli. In the rat these cells are located in a discrete region of the nucleus lying immediately rostral to the dorsal lateral geniculate nucleus (LGNd), where the visual field is represented in a retinotopic fashion. After injections of horseradish peroxidase (HRP) into this area, neurones labelled with reaction product were found in the LGNd and not in other thalamic relay nuclei. After HRP injections into the LGNd, labelled RNT cells were found only within the region which contains neurones responsive to photic stimuli. These observations suggest that there is a precise reciprocal relation between the two areas.Studies and comparisons of the responses of relay cells (P cells) in LGNd and cells in RNT to electrical shocks lead us to conclude that RNT cells receive their excitation mainly via those relay cells in LGNd which are themselves excited by fast-conducting retinal ganglion cell axons. Such cells in LGNd have phasic responses and concentric receptive fields while RNT cells have phasic responses and on/off fields and a comparison of the receptive field sizes of P cells and RNT cells suggests that only a small number of LGNd relay cells converge on to each RNT cell. Further, although a particular functional class of relay cells in LGNd (Y-type) is shown to provide the major input to visually responsive RNT cells, both Y type and W type relay cells are subject to their inhibitory control. These results furnish evidence that cells in the RNT have an important role in modulating the flow of visual information from the LGNd to cortex.     

Relation of cortical areas MT and MST to pursuit eye movements. I. Localization and visual properties of neurons

1. Among the multiple extrastriate visual areas in monkey cerebral cortex, several areas within the superior temporal sulcus (STS) are selectively related to visual motion processing. In this series of experiments we have attempted to relate this visual motion processing at a neuronal level to a behavior that is dependent on such processing, the generation of smooth-pursuit eye movements. 2. We studied two visual areas within the STS, the middle temporal area (MT) and the medial superior temporal area (MST). For the purposes of this study, MT and MST were defined functionally as those areas within the STS having a high proportion of directionally selective neurons. MST was distinguished from MT by using the established relationship of receptive-field size to eccentricity, with MST having larger receptive fields than MT. 3. A subset of these visually responsive cells within the STS were identified as pursuit cells--those cells that discharge during smooth pursuit of a small target in an otherwise dark room. Pursuit cells were found only in localized regions--in the foveal region of MT (MTf), in a dorsal-medial area of MST on the anterior bank of the STS (MSTd), and in a lateral-anterior area of MST on the floor and the posterior bank of the STS (MST1). 4. Pursuit cells showed two characteristics in common when their visual properties were studied while the monkey was fixating. Almost all cells showed direction selectivity for moving stimuli and included the fovea within their receptive fields. 5. The visual response of pursuit cells in the several areas differed in two ways. Cells in MTf preferred small moving spots of light, whereas cells in MSTd preferred large moving stimuli, such as a pattern of random dots. Cells in MTf had small receptive fields; those in MSTd usually had large receptive fields. Visual responses of pursuit neurons in MST1 were heterogeneous; some resembled those in MTf, whereas others were similar to those in MSTd. This suggests that the pursuit cells in MSTd and MST1 belong to different subregions of MST.     

The properties of the binocular receptive fields of lateral geniculate neurons

Summary The majority of cells in the dorsal nucleus of the lateral geniculate body (LGNd) in the cat have two receptive fields: one for each eye. Of the cells tested for binocularity (113), only 21 (18%) were purely monocular. The remainder had receptive fields for the non-dominant eye, the great majority of which (81 or 88%) were purely inhibitory and only 11 (12%) were excitatory. Cells with receptive fields for the non-dominant eye were found in all three laminae (A, A₁ and B) of the LGNd. The proportion of inhibitory receptive fields for the non-dominant eye was slightly greater when the dominant eye was ipsilateral (77%) than when it was contralateral (68%). The distribution of the binocular receptive field pairs about points of exact correspondence in the visual field had a standard deviation of about 0.9° in both horizontal and vertical directions.The properties of the inhibitory receptive fields were studied with moving slits of light and stationary flashing spots. Most of the fields were purely inhibitory and varied in size from 1.5° to 6° across. There were no specific stimulus requirements other than a change in contrast within the receptive field. The inhibitory effect was usually fairly weak, the spontaneous discharge of the neuron being inhibited much more readily than the driven discharge. The latency of the inhibition to a stationary flashing spot was about 50 msec, the inhibition was maximal about 20 msec after the onset and lasted up to about 400 msec.Binocular inhibition is not mediated by a corticogeniculate pathway from the visual areas since it survives removal of areas 17, 18 and 19 and the middle suprasylvian gyrus. It was concluded that the most likely mechanism was via interneurons whose axons cross the borders from one cell layer to another.     

Response properties and functional organization of neurons in midline region of medullary reticular formation of cats

Extracellular single-unit recordings were made in the anesthetized cat from neurons within the medullary raphe nuclei and nearby reticular formation. The descending axons from some of these neurons were characterized in terms of length, conduction velocity, and location within the white matter of the spinal cord. The sensory properties were characterized following somatic, baroreceptor, visual, and auditory stimuli. The mean conduction velocities of the descending axons from neurons in the medullary raphe nuclei and in the magnocellular tegmental field (26 m/s) were significantly slower than the mean conduction velocities of units in the regions immediately dorsal to them (50 m/s). Action potentials in neurons in the medullary raphe nuclei and in the magnocellular tegmental field were evoked by anti-dromic stimulation from the dorsolateral portion of the spinal cord (30 of 43, 70%), whereas neurons located in more dorsal regions along the midline and in the reticular formation projected into the ventral columns (18 of 25, 72%). Neurons were most easily activated by a tap stimulus to the body surface. This stimulus activated 84% of the neurons tested. The receptive fields were large, often including the four limbs, back, and head. Tap-sensitive neurons were found throughout the regions investigated. Stimulation of hair receptors activated 37% of neurons tested, whereas 19% responded to a high-intensity cutaneous stimulus (pinch), 35% responded to baroreceptor stimuli, 32% responded to visual stimuli, and 33% responded to auditory stimuli. Neurons responsive to pinch were likely to respond to baroreceptor stimuli and unlikely to respond to visual stimuli. Neurons responsive to visual stimuli were likely to respond to auditory stimuli.     

A correlation of receptive field properties with conduction velocity of cells in the rat's retino-geniculo-cortical pathway

1. The receptive field properties and responses to electrical stimulation of 126 P-cells recorded from the dorsal lateral geniculate nucleus (LGNd) were studied in the hooded rat. 2. Eighty-five cells had a concentric (Kuffler, 1953) receptive field organisation (46 off-centre on-surround; 39 on-centre off-surround). Of the remaining cells 29 had co-extensive on/off excitatory discharge regions, nine had on-centres with suppressive surrounds and two cells gave on-responses but had no suppressive surround. One cell was identified as suppressed-by-contrast. 3. On the basis of the battery of tests developed for the identification of cell types in the cat's retina and LGNd, 35 of the cells with a Kuffler-type receptive field organisation were identified as Y-like. The majority of the remaining cells, both concentric and others, reminded us of the different subclasses of W-cells of the cat. Nine concentric cells in most of the tests exhibited X-like properties. 4. All of the Y-like cells were driven by relatively fast conducting retinal ganglion cell axons, comprising the t1 conduction velocity group. The majority of the remaining cells were driven by slower axons comprising t2 or t3 conduction velocity groups. 5. Thus, in the rat, as in other mammalian species studied so far, there is a correlation between the conduction velocity groups in the retino-geniculo-cortical pathway and the functional groups based on the cells' receptive field properties. There seem to be functional equivalents of the cat's Y- and W-cell classes but evidence for a distinct X-like class of cells is lacking.     

Effect of passive eye movement on retinogeniculate transmission in the cat

1. The nature and time window of interaction between passive phasic eye movement signals and visual stimuli were studied for dorsal lateral geniculate nucleus (LGNd) neurons in the cat. Extracellular recordings were made from single neurons in layer A of the left LGNd of anesthetized paralyzed cats in response to a normalized visual stimulus presented to the right eye at each of several times of movement of the left eye. The left eye was moved passively at a fixed amplitude and velocity while varying the movement onset time with respect to the visual stimulus onset in a randomized and interleaved fashion. Visual stimuli consisted of square-wave modulated circular spots of appropriate contrast, sign, and size to elicit an optimal excitatory response when placed in the neurons' receptive-field (RF) center. 2. Interactions were analyzed for 78 neurons (33 X-neurons, 43 Y-neurons, and 2 physiologically unclassified neurons) on 25-65 trials of identical visual stimuli for each of eight times of eye movement. 3. Sixty percent (47/78) of the neurons tested had a significant eye movement effect (ANOVA, P less than 0.05) on some aspect of their visual response. Of these 47 neurons, 42 (89%) had a significant (P less than 0.05) effect of an appropriately timed eye movement on the number of action potentials, 36 (77%) had a significant effect on the mean peak firing rate, and 31 (66%) were significantly affected as evaluated by both criteria. 4. The eye movement effect on the neurons' visual responses was primarily facilitatory. Facilitation was observed for 37 (79%) of the affected neurons. For 25 of these 37 neurons (68%), the facilitation was significant (P less than 0.05) as evaluated by both criteria (number of action potentials and mean peak firing rate). Ten (21%) of the affected neurons had their visual response significantly inhibited (P less than 0.05). 5. Sixty percent (46/78) of the neurons were tested for the effect of eye movement on both visually elicited activity (visual stimulus contrast = 2 times threshold) and spontaneous activity (contrast = 0). Eye movement significantly affected the visual response of 23 (50%) of these neurons. However, spontaneous activity was significantly affected for only nine (20%) of these neurons. The interaction of the eye movement and visual signals was nonlinear. 6. Nine of 12 neurons (75%) tested had a directionally selective effect of eye movement on the visual response, with most (8/9) preferring the temporal ward direction.(ABSTRACT TRUNCATED AT 400 WORDS)     

Receptive-field properties of transcallosal visual cortical neurons in the normal and reeler mouse

The receptive-field properties of neurons in the striate visual cortex of normal and reeler mutant mice were studied with single-unit recording methods in order to determine whether the connections underlying these properties are altered by the developmental abnormality in neuronal position that characterizes reeler neocortex. Neurons with a projection through the corpus callosum were selected for study because they form a physiologically identifiable class of visual cortical neurons with a characteristic distribution of receptive-field properties that can be compared for normal and reeler cortex. Transcallosal cortical neurons in area 17 near its border with area 18a were identified by antidromic stimulation delivered through bipolar electrodes in the contralateral cortex. A computer controlled the visual stimuli, data acquisition, and analysis. Transcallosal neurons were principally found in layers II-III and V in the normal cortex and in a broand band deep in the reeler cortex. These populations had similar distributions of antidromic latencies, indicating that the neurons sampled from normal and reeler cortex were taken from populations with similar axonal diameters and soma sizes. The receptive-field properties of 46 units in 22 normal mice and 28 units in 11 reeler mice were characterized. Transcallosal neurons in both normal and reeler cortex were usually binocularly responsive and dominated by input from the contralateral eye. They exhibited either nonoriented (31 and 48%, respectively) or oriented (69 and 52%) receptive fields. Tuning 10 stimulus velocity was broad, with peak velocity sensitivities ranging from 1 to 1,000 degrees/s. Directional selectivity was present in 41% of normal units ad 32% of reeler units. There was no significant difference between normal and reeler cortex in the distribution of these properties. Transcallosal neurons were also examined for the presence of an inhibitory surround by comparing their responses to moving or stationary stimuli of varying sizes. Of the tested neurons, most (11/17 in normal cortex, 6/9 in reeler) showed evidence of a decrease in response to large moving stimuli. A large proportion (16/20) of normal neurons tested with stationary flashing stimuli had some degree of surround inhibition whereas significantly fewer (5/17) neurons in reeler cortex had this property. Thus, transcallosal neurons in reeler cortex less frequently had an inhibitory surround demonstrable with stationary flashing stimuli, but this difference between normal and reeler was not apparent with a moving stimulus.(ABSTRACT TRUNCATED AT 400 WORDS)     

Efferent neurons and suspected interneurons in S-1 vibrissa cortex of the awake rabbit: receptive fields and axonal properties

1. The behavioral tractability of the rabbit was exploited and enabled, in the fully awake state, receptive-field analysis of antidromically identified efferent neurons within the vibrissa representation of primary somatosensory cortex (S-1). Efferent neurons studied included ipsilateral corticocortical neurons (C-IC neurons, n = 56) that project to or beyond the second somatosensory cortical area (S-2) and corticofugal neurons of layer 5 (CF-5 neurons, n = 75) and layer 6 (CF-6 neurons, n = 92) that project to and/or beyond the thalamus. 2. An additional class of neurons was studied that was not activated antidromically from any stimulus site, but which responded synaptically to electrical stimulation of the ventrobasal (VB) thalamus with a burst of three or more spikes at frequencies of 600 to greater than 900 Hz. Most of these neurons also responded synaptically to stimulation of S-2. The action potentials of these neurons were much shorter (mean = 0.43 ms), than those of efferent neurons (mean = 0.98 ms). Such properties have been associated with interneurons found throughout the central nervous system, and these neurons are thereby referred to as suspected interneurons (SINs). Although SINs were found at all cortical depths, a strong peak in the distribution occurred just superficial to the peak in the distribution of CF-5 neurons. Most SINs located within this peak responded to deflection of only a single vibrissa. In contrast, SINs located in layer 6 and in layer 2-3 responded to deflection of many vibrissae (median = 11.0 and 5.5 vibrissae, respectively). In addition, SINs of layer 6 and layer 2-3 had significantly longer synaptic latencies to stimulation of VB thalamus than did SINs located at intermediate cortical depths. 3. The properties of efferent neurons and SINs differed considerably. Efferent neurons never responded to stimulation of VB thalamus with the high-frequency burst of spikes characteristic of SINs. Although greater than 70% of CF-6, CF-5 and C-IC neurons had receptive fields that were directionally selective, only 20% of SINs showed any degree of directional selectivity. Furthermore, SINs showed both much lower angular thresholds to vibrissa deflection and a much greater ability to follow high-stimulus frequencies than was seen in efferent neurons. The spontaneous firing rates of SINs had a mean value of 16.5 spikes/s, which was the highest seen in any population within S-1. 4. CF-5 neurons had a number of properties which contrasted with those of both CF-6 and C-IC neurons.(ABSTRACT TRUNCATED AT 400 WORDS)     

Response properties of area 17 neurons in cats reared in stroboscopic illumination

The response properties of 196 area 17 cells were studied qualitatively in seven cats reared from birth in a stroboscopically illuminated environment (frequency, 2/s; duration, 200 microseconds). Quantitative testing with the multihistogram technique was carried out in 115 cells. As control population, 453 neurons recorded in area 17 of the normal adult cat and tested qualitatively (of which 301 neurons were tested quantitatively) were available. In area 17 of strobe-reared cats, a number of spatial characteristics of receptive fields investigated with hand-held stimuli were found to be abnormal. There was a strong reduction in the encounter frequency both of end-stopped cells and of binocularly driven cells in the strobe-reared cats. Central receptive fields in strobe-reared cats were wider than in normal cats, but the increase in receptive-field width with eccentricity was still observed. More cells than in normal cats showed either no selectivity or only a weak bias for stimulus orientation, but the orientation tuning of orientation-selective cells was similar in strobe-reared and normal cats. Quantitative testing revealed that the velocity preference of cells in area 17 subserving central vision was different in strobe-reared cats from that of normal cats, due to a reduction in the encounter frequency of cells showing a preference for low velocities. There was no difference in velocity preference between strobe-reared and normal cats in the parts of area 17 that subserve peripheral vision, the proportion of neurons responding to fast velocities showing a similar increase in both groups of animals. Fewer cells were direction selective in strobe-reared cats than in normal cats. Most of the remaining direction-selective cells had peripheral receptive fields and the synergism between leaving an OFF subregion and entering an ON subregion contributed to their direction selectivity. Latency of neurons in area 17 of strobe-reared cats was slightly higher than in normal cats, but the response strength of neurons was the same in the two groups. The proportion of cells failing to respond to briefly flashed stationary stimuli was significantly lower in strobe-reared than in normal animals. Qualitative and quantitative testing showed that strobe rearing has a stronger effect on the parts of area 17 that subserve central vision than on those that subserve peripheral vision. Comparing the present results with those of Kennedy and Orban (37) shows that strobe rearing has less effect on area 17 than on area 18 and that the functional differences between areas 17 and 18 in strobe-reared cats are smaller than in normal cats.     

Visual field projection columns and magnification factors in the lateral geniculate nucleus of the cat

Summary The precision of the projection of the visual field to the dorsal lateral geniculate nucleus (LGNd) of the cat was studied by plotting the receptive fields of single neurons recorded extra-cellularly in the nucleus. The concepts of a projection column and of random scatter in the location of receptive fields have been defined in relation to cells in the LGNd. A projection column contains 90% of all the cells in the LGNd that have receptive fields with a common visual direction, the central axis of the column being the projection line for the given visual direction. In the region of the LGNd devoted to central vision the columns have a circular cross section and are about 1 mm in diameter.The projections of adjacent areas of visual field (and hence of the retina) overlap extensively in the LGNd. In this study, the overlap of retinal afferents in the LGNd was measured in terms of the random scatter of receptive field positions for cells recorded in a given electrode penetration parallel to projection columns in the nucleus. The monocular receptive field scatter within a column in the LGNd is about of the same magnitude as both the monocular receptive field scatter within a cortical column and the binocular receptive field disparities of cortical units.The differential magnification of the visual field on the LGNd is a reflection of the ganglion cell density differences in the retina.