Response characteristics of neurons in the pulvinar of awake cats to saccades and to visual stimulation

We studied responses of pulvinar neurons in awake cats that were allowed to execute spontaneous eye movements. Extracellular cell activity during saccades, saccade-like image shifts, and various stationary visual stimuli was recorded together with the animals' eye positions. All neurons analyzed had receptive fields that covered most of the central 80x80 degrees of the animals' visual field and did only respond to large (>20 degrees) visual stimuli. According to their response properties, recorded neurons were divided into three populations. The first group, termed "S neurons" (16%), responded when the animals performed saccades but were unresponsive to any of the visual stimuli tested. These neurons do not seem to receive a visual input that is strong enough to drive them. The second group, termed "V neurons" (51%), responded to various visual stimuli including saccade-like image motion when the eyes were stationary, but not when the animals executed saccades. V neurons therefore distinguish retinal image movements that are generated externally from internally generated image motion. Finally, "SV neurons" (31%) responded when the animals made saccades as well as to saccade-like image motion or to stationary stimuli. Although these neurons do not distinguish self-induced retinal image motion from motion generated by external stimulus movements, they must receive non-retinal motion-related input, because responses elicited by saccades had shorter latencies than responses to saccade-like stimulus movements. Only SV neurons resemble response properties of pretectal neurons that project to the pulvinar and that comprise the major subcortical visual input. The functional significance of pulvinar neuronal populations for visual and visuomotor information processing is discussed.     

Organization of receptive fields of tonic and phasic neurons of the pulvinar in the cat

The receptive fields (RF) of 163 neurons of the pulvinar were investigated by the method of point testing the RF surface with a stationary, flashing light spot. The RFs of 26% of the neurons were characterized by a phasic pattern of response in all regions studied, while the RFs of 15% of the neurons consisted of only tonic elements. A complex RF organization, consisting of tonic and phasic subfields, was characteristic of 59% of the neurons. On the basis of this fact the postulate is advanced concerning the convergence of two types of afferents on a single pulvinar neuron. The cell population receiving inputs from purely tonic or purely phasic afferents comprises 41% of all cells investigated. The measurement of the latent periods of neuron responses to a stationary, flashing light spot showed that neurons with a phasic type of response are distinguished by a shorter latent period compared to neurons with tonic and mixed types of responses.Translated from Fiziologicheskii Zhurnal SSSR imeni I. M. Sechenova, Vol. 69, No. 1, pp. 19–25, January, 1983.     

Pulvinar nuclei of the behaving rhesus monkey: visual responses and their modulation

We have examined the properties of neurons in three subdivisions of the pulvinar of alert, trained rhesus monkeys 1) an inferior, retinotopically mapped area (PI), 2) a lateral, retinotopically organized region (PL), and 3) a dorsomedial visual portion of the lateral pulvinar (Pdm), which has a crude retinotopic organization. We tested the neurons for visual responses to stationary and moving stimuli and for changes in these responses produced by behavioral manipulations. All areas contain cells sensitive to stimulus orientation as well as neurons selective for the direction of stimulus movement; however, the majority of cells in all three regions are either broadly tuned or nonselective for these attributes. Nearly all cells respond to stimulus onset, a significant number also give a response to stimulus termination, and rarely a cell gives only off responses. Nearly all cells increase their discharge rate to visual stimuli. Receptive fields in the two retinotopically mapped regions, PI and PL, have well-defined borders. The sizes of these receptive fields show a positive correlation with the eccentricity of the receptive fields. The receptive fields in the remaining region, Pdm, are frequently very large, but with these large fields excluded, show a similar correlation with eccentricity. All pulvinar cells tested (n = 20) were mapped in retinal coordinates; the receptive fields are positioned in relation to the retina. We found no cells with gaze-gated characteristics (2), nor cells mapped in a spatial coordinate system. The response latencies in PI and PL are shorter and less variable than the latencies in Pdm. Active use of a stimulus can produce an enhancement or attenuation of the visual response. Eye-movement modulation was found in all three subdivisions in about equal frequencies. Attentional modulation was common in Pdm and was rare in PI and PL. The modulation is spatially selective in Pdm and nonselective in PI for a small number of tested cells. These data demonstrate functional differences between Pdm and the other two areas and suggest that Pdm plays a role in selective visual attention, whereas PI and PL probably contribute to other aspects of visual perception.     

Gating and control of primary visual cortex by pulvinar

The primary visual cortex (V1) receives its driving input from the eyes via the lateral geniculate nucleus (LGN) of the thalamus. The lateral pulvinar nucleus of the thalamus also projects to V1, but this input is not well understood. We manipulated lateral pulvinar neural activity in prosimian primates and assessed the effect on supra-granular layers of V1 that project to higher visual cortex. Reversibly inactivating lateral pulvinar prevented supra-granular V1 neurons from responding to visual stimulation. Reversible, focal excitation of lateral pulvinar receptive fields increased the visual responses in coincident V1 receptive fields fourfold and shifted partially overlapping V1 receptive fields toward the center of excitation. V1 responses to regions surrounding the excited lateral pulvinar receptive fields were suppressed. LGN responses were unaffected by these lateral pulvinar manipulations. Excitation of lateral pulvinar after LGN lesion activated supra-granular layer V1 neurons. Thus, lateral pulvinar is able to powerfully control and gate information outflow from V1.     

Organization of receptive fields in the forebrain ofEmys orbicularis

Interaction between circumscribed areas of the receptive field of visual cortical neurons was investigated in the turtle forebrain. The neurons of the superficial cortical strata summate excitation arriving from different points of the receptive field. Interaction between local areas of the receptive field of deep cortical neurons depends essentially on the distance between the interacting points.Pharmacological blocking (KC1, GABA) of circumscribed areas of the forebrain cortex suppresses the circumscribed areas of tne receptive field of deep cortical neurons. Thus it is deduced that the cortex of the turtle's forebrain contains representations of the local areas of the retina, even though these neurons have extensive receptive fields. This deduction is confirmed by the fact that among the optic fibers entering the cortex, there are single fibers with receptive fields of between 2 and 5.     

Differential effects of GABA and bicuculline on rapidly- and slowly-adapting neurons in primary somatosensory cortex of primates

Summary In cortical area 3b of monkeys, responses of 71 single neurons to controlled indentations of glabrous skin were recorded before and during iontophoretic application of GABA and bicuculline methiodide (BMI), a GABA receptor antagonist. Constant amplitude indentations were applied to selected sites within the receptive fields of neurons representing the glabrous skin on the digits and palm. Profiles of response magnitudes across stimulation sites were used to quantify receptive field dimensions before and during antagonism of GABAergic inhibition. During administration of BMI, the receptive fields of 26 rapidly-adapting neurons were increased by 3–4 times their original size. Response latencies were substantially longer in the region of expansion than in the original receptive field, suggesting that expansion might be mediated by intracortical connections. The expansion of RFs onto adjacent digits after blockade of GABAergic inhibition suggests that somatotopic reorganization following digit amputations may be subserved by existing excitatory connections. The responses of slowly-adapting neurons were separated into two components, a dynamic response corresponding to activity elicited by the initial indenting ramp and a static response produced by the sustained indentation. Among 8 slowly-adapting neurons tested with BMI, the receptive fields of the dynamic response component increased to an extent that was similar to the change produced in rapidly-adapting neurons. By contrast, the static response component was rarely altered by BMI. Comparison of the responses to administration of GABA revealed that only 12 of 27 slowly-adapting neurons were inhibited in a dose-dependent manner, whereas 37 of 44 rapidly-adapting neurons exhibited significant reduction of responses in the presence of GABA. Hypotheses are proposed to explain the differential effect of BMI and GABA on slowly- and rapidly-adapting cortical neurons.     

Rat somatosensory (SmI) cortex: II. Laminar and columnar organization of noxious and non-noxious inputs

Summary The laminar and columnar organization of the rat SmI cortex was investigated under halothanenitrous oxide anaesthesia during microelectrode penetrations perpendicular to the cortical surface, using histological reconstruction of the electrode tracks. Neurons were studied in terms of receptive field properties (see companion paper) and laminar distribution. Neurons driven by non-noxious cutaneous stimulation and others by non-noxious deep stimulation, applied on contralateral receptive fields, could be recorded in the same penetration. Modality specific penetrations were observed in 48% of cases only. This finding suggests that there is little submodality segregation in the rat SmI cortex. Receptive fields successively observed in a given penetration were usually overlapping. Modality-specific columns were less often observed than place-specific columns during radial penetrations. Neurons driven by non-noxious stimulation as well as neurons driven by noxious stimulation could be recorded successively in the same penetration. Neurons driven by non-noxious cutaneous stimulation were found in layers II to V and were rare in layer VI. In contrast, nociceptive specific neurons were found almost exclusively in layers Vb and VI and convergent neurons in layer V. The size of the receptive fields was a function of the laminar position of the neurons: receptive fields were, on the average, small in layer IV, larger in layer II–III and V and even larger in layer VI. The somatotopic organization of the receptive fields of neurons driven by noxious stimulation was different from that of neurons driven by non-noxious stimulation. Such a difference was due in part to the larger size of the receptive fields of the neurons driven by noxious stimulation and also to their different topographical organization. These results provide new data concerning the functions of the rat SmI cortex. Namely they show that the cortical processing of somatic non-noxious and noxious inputs is based on laminar as well as columnar patterns of organization.Supported by DGRST (DN/80.7.0236)Chercheurs INSERM     

Model Studies of the Mechanisms of Tuning of Visual Cortex Neurons to Incomplete Cross-Shaped Figures

Numerical simulation modeling of the receptive fields of visual cortex neurons able to detect cross-shaped figures with masked central or peripheral areas was performed. Receptive field models of two types were considered: those with antagonistic and cooperative interactions between the center and the periphery. Model neurons with receptive fields with reciprocal (antagonistic) interactions produced greater responses to peripheral or central crosses than to complete crosses. Studies using the model showed that the basis of this type of tuning could be provided by a disinhibition mechanism: blockade of the inhibitory zones in the center or periphery of the receptive field by activation of a lateral disinhibitory zone. A model with cooperative interactions between the center and periphery of the receptive field was also studied, in which responses to complete crosses were summed from the responses to the peripheral and central parts. Tuning of these model receptive fields was comparable to the sensitivity of real visual cortex neurons to the shape, size, and orientation of figures. The properties of model receptive fields (configuration, localization, and weightings of the various zones) allowing simulation of the properties of cat visual cortex field 17 neurons sensitive to the orientation and configuration of incomplete cross-shaped figures were identified.     

Effects of frontal eye field stimulation upon activities of the lateral geniculate body of the cat

Summary Effects of electrical stimulation of the frontal eye field (FEF) upon activities of the lateral geniculate body (LG) were studied in encéphale isolé cats. In some experiments the effects were examined by recording field responses of the dorsal nucleus of LG (LGd) and the visual cortex (VC) to electrical stimulation of the optic chiasm (OX). Conditioning repetitive stimulation of FEF exerted no significant effects on the r₁ wave of LGd responses but had a facilitatory effect on the r₂ wave. FEF-induced facilitation of VC responses was prominent in the late postsynaptic components. These effects had latencies of 50–100 msec and durations of 200–500 msec. Transection of the midbrain showed that most of the FEF-effect was not mediated via the brainstem reticular formation.Extracellular unitary recordings were made from 125 neurons, of which 91 were LGd neurons, 23 neurons of the caudal part of the thalamic reticular nucleus (TRc) and 11 neurons of the ventral nucleus of LG (LGv). In 30 of 87 LGd relay neurons FEF stimuli increased response probabilities to OX stimuli and their spontaneous discharges. These FEF-facilitated LGd neurons were distinguished from the non-affected ones in that the former had longer OX-latencies than the latter. The FEF-facilitated neurons probably correspond to X neurons of LGd.In 17 TRc neurons the effects were inhibitory. Their time courses were similar to those of the facilitation in the LGd relay neurons. Seven LGv neurons received facilitatory effects from FEF. Among them 5 neurons showed short-latency (6.7–17 msec) responses to FEF single shocks.The FEF sites inducing conjugate lateral eye movements exerted stronger facilitatory effects than those inducing upward or centering eye movements did.It is suggested that the effects may subserve to cancel the inhibitory convergence onto X-cells just after saccadic eye movements so as to improve visual information transmission through LGd during the eye fixation.     

Transformation of the afferent tactile signal into a motor command in the cat motor cortex

Activity of 112 neurons of the precruciate motor cortex in cats was studied during a forelimb placing reaction to tactile stimulation of its distal parts. The latent period of response of the limb to tactile stimulation was: for flexors of the elbow (biceps brachii) 30–40 msec, for the earliest reponses of cortical motor neurons about 20 msec. The biceps response was observed 5–10 msec after the end of stimulation of the cortex with a series of pulses lasting 25 msec. Two types of excitatory responses of the neurons were identified: responses of sensory type observed to each tactile stimulation of the limb and independent of the presence or absence of motion, and responses of motor type, which developed parallel with the motor response of the limb and were not observed in the absence of motion. The minimal latent period of the responses of motor type was equal to the latent period of the sensory responses to tactile stimulation (20±10 msec). Stimulation of the cortex through the recording microelectrode at the site of derivation of unit activity, which increased during active flexion of the forelimb at the elbow (11 stimuli at intervals of 2.5 msec, current not exceeding 25 A), in 70% of cases evoked an electrical response in the flexor muscle of the elbow.Translated from Neirofiziologiya, Vol. 9, No. 2, pp. 115–123, March–April, 1977.     

Spatio-temporal interactions and the spatial phase preferences of visual neurons

Summary We recorded single neuron responses in the cat's lateral geniculate nucleus (LGN) and visual cortex to compound stimuli composed of two sinusoidal gratings in a 21 frequency ratio. To probe visual receptive field symmetry, we varied the relative spatial phase of the two components and measured the effect on neuronal responses. We expected that on-center LGN neurons would respond best to gratings combined in positive cosine (bright bar) phase, while off-center LGN neurons would respond best to gratings combined in negative cosine (dark bar) phase. When drifting stimuli were used, cells' phase preferences were roughly 90 deg away from the expected values; when stationary, contrast-modulated stimuli were used, phase preferences were as originally predicted. Computer simulations showed that this discrepancy could be explained by taking into account the cells' temporal properties. Thus, tests using drifting stimuli confound the spatial structure of visual neural receptive fields with their temporal response characteristics. A small sample of data from cortical neurons reveals the same confound.     

Functional organization of the nociceptive withdrawal reflexes

Summary The spatial organization of the cutaneous input to hindlimb withdrawal reflexes was studied in spinalized, decerebrated, unanesthetized rats. Reflex activity in plantar flexors of the digits, pronators of the foot, dorsiflexors of the digits, and/or the ankle and flexors of the knee was recorded with electromyographic techniques for up to 12 h after spinalization. Graded mechanical (pinch) and thermal stimulation (CO₂ laser) of the skin were used. Reflexes were absent (spinal shock) during approximately 10–20 min after spinalization. The reflex thresholds for pinch and CO₂ laser stimulation then decreased considerably during the following 5–8 h. After this time, even mild pressure (less than 0.1 N/mm²) on the skin was sufficient to evoke a reflex in most muscles. During the period from about 0.5–3 h after spinalization, the nociceptive receptive field of each muscle usually corresponded to the area of the skin withdrawn by the muscle. Maximal responses were evoked from the area of the receptive field maximally withdrawn. During this period, responses to innocuous pinch were evoked mainly from the most sensitive area of the receptive fields. Concomitant with the decrease in reflex thresholds, the nociceptive receptive fields expanded for all muscles, often to include areas of the skin not withdrawn by the muscles. For most muscles, reflexes on tactile stimuli were eventually elicited from the entire receptive fields. The receptive fields for thermonociceptive and mechanonociceptive inputs were similar in most muscles. The interossei muscles were exceptional in that they responded very weakly to thermal stimulation. It is concluded that there are neuronal networks in the spinal cord that translate cutaneous nociceptive and tactile input into a withdrawal. However, the control exerted by descending pathways is necessary to maintain a functionally adequate excitability in these reflex pathways and an appropriate size for their receptive fields.     

Neurons of the superficial tectal gray an intracellular HRP-study on the kitten superior colliculus in vitro

Summary An en bloc preparation of the mammalian superior colliculus in vitro has been used to study neurons of the superficial gray layer (SGS) with intracellular recording and HRP-technics. Electrophysiological data from kittens at 4–19 days of age suggest that at this stage SGS-neurons possess multiple spike trigger zones which can be activated by synaptic depolarization and are probably located on dendrites. In response to intratectal stimulation SGS-neurons generate EPSP-IPSP sequences or IPSPs. IPSPs are found in all penetrated cells as early as the 4th postnatal day. Ascending projection cells (APCs) and inter-layer cells (ILCs) have been identified based on antidromic activation and/or intracellular labeling with HRP. The extended dendritic arbor of APCs and ILNs (dorsal spread up to 10–20 m below surface, horizontal spread up to 1100–1500 m) enables these cells to sample visual information from a wide area of the visual field. Recurrent collaterals, in conjunction with potent inhibitory mechanisms, could contribute to the formation of receptive field properties of superficial tectal neurons. ILCs establish collateral connections with the intermediate gray layer.     

Ontogenesis of receptive field characteristics in the dorsal lateral geniculate nucleus of the rabbit

Summary The responses of rabbit dorsal lateral geniculate neurons to light or optic nerve shock were tested for 415 units in 43 rabbit pups 2–20 days of age. Units were driven by optic nerve shock at the youngest ages tested, but could not be driven by light until postnatal day six. Examples of each of the three prominent categories of receptive fields found in the adult were first observed at 8 days of age. Cells with receptive field properties not characteristic of the dorsal lateral geniculate nucleus of the adult were encountered until 17 days of age. The percentage of neurons with uniform and motion sensitive receptive fields approached adult levels soon after eye opening (11–12 days) but the percentage of cells with concentric receptive fields showed a steady increase throughout the neonatal period studied. The relevance of our data to the development of the visual response in the dorsal lateral geniculate nucleus and striate cortex is discussed.     

Spatial arrangements of responses by cells in the cat visual cortex to light and dark bars and edges

Summary Detailed examination is made of the responses of visual cortical cells (area 17, border 17–18 and adjacent area 18) in the anaesthetized cat to stationary flashing bars and to bars (lines) and edges moving at their optimal velocities. Particular attention is given to the receptive field organization of cells in the simple family. While there is good general agreement between the main receptive field subregions revealed by stationary and moving stimuli, the responses to moving light and dark bars, supplemented by the responses to moving light and dark edges, provide a much more rapid, accurate and complete guide to the spatial organization of the receptive fields than do the response profiles to a stationary flashing bar. Moving light and dark bars between them generally reveal more subregions in the receptive fields of simple cells than is evident from the response profiles to a stationary flashing bar, particularly when the receptive fields have many subregions. In addition the responses to moving edges provide a rapid guide to spatial summation across the width of a subregion and the possible antagonistic effects of the next subregion in sequence.Two subclasses of cells in the simple family have been recognized: ordinary simple and fast simple cells. Two cell classes (A-cells and silent periodic cells) having properties intermediate between simple and complex types are discriminated and their properties described.     

Connections between the pulvinar complex and cytochrome oxidase-defined compartments in visual area V2 of macaque monkey

We examined the distribution of pulvinar afferents to visual area V2 of macaque monkey cerebral cortex in relation to the distribution of the metabolic enzyme cytochrome oxidase (CO). V2 contains three sets of stripelike subregions that are marked by differential staining for CO, and which have different corticocortical connections. The pulvinar provides the major subcortical input to V2, and this input is known to be patchy. We were interested to determine how the pattern of pulvinar afferents relates to the layout of the three stripelike compartments that characterize V2. We made large injections of WGA-HRP into the pulvinar (labelling both the inferior and lateral divisions) and mapped the resulting orthograde terminal and retrograde cell label within V2. We observed pulvinar terminal label mainly in lower layer 3 (at the layer 4 border), with light label in layer 1 as well; terminal label in layers 3–4 was distributed in discrete patches with faint bridges of light label between. Comparison with adjacent sections stained for CO or Cat-301 showed that pulvinar terminal zones aligned precisely with regions of increased CO staining, and targeted both thick (Cat-301⁺) and thin CO-rich stripes, avoiding the pale stripes (which aligned with the faint bridges of terminal label). Retrogradely labelled cells were found in layers 5A and 6, but the bulk of the feedback to pulvinar arose from layer 6 rather than layer 5 (unlike V1, where feedback to pulvinar arises primarily from layer 5B). These results show that the increased CO staining in certain subregions of V2 is closely correlated with the presence of thalamic terminals from the pulvinar. Although we cannot rule out the possibility that different sets of pulvinar neurons project to different CO compartments in V2, the presence of a prominent thalamic input shared by the thick and thin CO stripes (which receive different V1 afferents and make different feedforward projections to other visual cortical areas) could underlie the preferential intrinsic interconnections shown to exist between these V2 subregions and suggests another potential source of integration between the two cortical visual streams.     

Functional organization in the cat's pulvinar complex

Summary The responses of 192 single units in the cat's pulvinar-complex, comprising the inferior, medial and lateral pulvinar nuclei, were studied in paralysed cats, lightly anaesthetized with N₂O/O₂ supplemented with pentobarbitone. About 60% of the cells were visually driven and their receptive fields classified as either diffuse, concentric, movement sensitive, direction sensitive or orientation sensitive. The response fields of such cells were commonly large. Response field maps for the movement and direction sensitive cells formed a heterogenous population with uniform on-off fields to more complex arrangements with on- or off-centres, often with only partial surrounds; other cells responded exclusively to moving stimuli.A dual representation of the visual field was found in the pulvinar-complex corresponding to the striate and tectal recipient zones described anatomically by others. The representation in the striate recipient zone comprised an oblique column running medio-laterally and rostrocaudally through the inferior pulvinar and lateral margin of the medial pulvinar. The peripheral visual field was represented laterally and the vertical meridian medially; the upper visual field was represented dorso-laterally in the medial pulvinar and the lower visual field caudo-ventrally within the inferior pulvinar. That this visuotopic organization corresponded to the striate recipient zone was established by tracing the retrograde transport of HRP. Medial to the striate zone evidence for a second visual field representation was found, apparently more randomly organized than the striate zone, corresponding to the presumed tectal recipient zone. These results support the assertion that cytoarchitectural boundaries do not necessarily delineate functional (visuotopically organized) regions. These observations suggest caution when comparing cytoarchitecturally defined regions between species; rather, functionally equivalent regions should be compared.Formerly the Research Department of Communication     

The inhibitory components in the responses of the lateral suprasylvian area neurons to moving stimuli in cats

The inhibitory components in the neuronal responses of the cat's lateral suprasylvian area (LSA) to moving bright and dark stimuli were investigated. The LSA neurons could be divided into two groups. Neurons of the first group (33%) do not reveal spatial displacement of the inhibitory zones and show displacement of the discharge centers in the receptive field only for one polarity of contrast of moving stimuli, either brighter or darker than the background. The second group (67%) contained the neurons which showed a spatial displacement of the inhibitory components and discharge centers in the receptive field for either polarity of contrasts of the moving stimuli. Tested with stationary flashing stimuli, the majority of neurons in both groups had overlapping ON-OFF discharge regions within their receptive fields. The results obtained with moving stimuli of different speeds and with the masking method suggest the rebound origin of the inhibitory responses in LSA neurons.     

Organization and properties of visually responsive neurones in the suprageniculate nucleus of the cat

Summary Visually responsive neurones of the cat's suprageniculate nucleus were categorized according to their responses to a variety of different types of light stimuli. Their velocity preferences were assessed quantitatively and have been found to predominate in the high range. The positions and dimensions of their receptive fields were determined and these tended to be found within a zone between the vertical meridian and 30–35°. Receptive fields had mean diameters smaller than those reported by others for the pulvinar-LP complex. From these and other electrophysiological data, inferences have been made of the likely sources of afferents providing visual driving. A proposal is offered for SGn visuotopic organization based on correlations of receptive field location with cell position, as determined through electrode track reconstructions.     

The effects of light-adaptation on rod and cone receptive field organization of monkey ganglion cells

1. Receptive fields of perifoveal ganglion cells have been measured by determining threshold for eliciting a just detectable response using either concentric spot stimuli centred on the receptive field or small spot stimuli in different parts of the receptive field at various states of retinal adaptation and with stimuli selected to separate rod from cone function.2. Light-adaptation decreases the sensitivity, latency and duration of threshold responses throughout the receptive field of a ganglion cell.3. With all patterns of retinal stimulation and states of adaptation, threshold signals of the rods reach a ganglion cell later and those of the cones earlier than approximately 50 msec after a light stimulus.4. In the more dark-adapted retina threshold rod and cone signals can be transmitted to the brain by the same or by neighbouring ganglion cells but not simultaneously; in the light-adapted state only the cone signal is transmitted.