Non-directional Cells Research Articles

Evidence for two distinct thalamocortical circuits in retrosplenial cortex

Retrosplenial cortex (RSC) lies at the interface between sensory and cognitive networks in the brain and mediates between these, although it is not yet known how. It has two distinct subregions, granular (gRSC) and dysgranular (dRSC). The present study investigated how these subregions differ with respect to their electrophysiology and thalamic connectivity, as a step towards understanding their functions. The gRSC is more closely connected to the hippocampal formation, in which theta-band local field potential oscillations are prominent. We, therefore, compared theta-rhythmic single-unit activity between the two RSC subregions and found, mostly in gRSC, a subpopulation of non-directional cells with spiking activity strongly entrained by theta oscillations, suggesting a stronger coupling of gRSC to the hippocampal system. We then used retrograde tracers to test for differential inputs to RSC from the anteroventral thalamus (AV). We found that gRSC and dRSC differ in their afferents from two AV subfields: dorsomedial (AVDM) and ventrolateral (AVVL). Specifically: (1) as a whole AV projects more strongly to gRSC; (2) AVVL targets both gRSC and dRSC, while AVDM provides a selective projection to gRSC, (3) the gRSC projection is layer-specific: AVDM targets specifically gRSC superficial layers. These same AV projections are topographically organized with ventral AV neurons innervating rostral RSC and dorsal AV neurons innervating caudal RSC. These combined results suggest the existence of two distinct but interacting RSC subcircuits: one connecting AVDM to gRSC that may comprise part of the cognitive hippocampal system, and the other connecting AVVL to both RSC regions that may link hippocampal and perceptual regions. We suggest that these subcircuits are distinct to allow for differential weighting during integration of converging sensory and cognitive computations: an integration that may take place in thalamus, RSC, or both.

Cartesian and non-Cartesian responses in LGN, V1, and V2 cells

Cell responses to drifting Cartesian (parallel) and non-Cartesian (concentric, radial, and hyperbolic) stimuli were recorded in and beyond the classical receptive field (CRF) in the lateral geniculate nucleus (LGN), V1, and V2 of anesthetized monkeys. Many cells were equally responsive to Cartesian and non-Cartesian, especially concentric, gratings. Around 15% of cells in each area were significantly more responsive to concentric compared to parallel gratings; however, cells significantly more responsive to parallel compared to concentric gratings were more numerous in the cortex. While many cells responded to hyperbolic and radial gratings, few were most responsive to these gratings. Cell selectivity decreased for Cartesian and increased for non-Cartesian gratings from V1 to V2 and the relative response varied as a function of stimulus extent with respect to the CRE. Complex, nonoriented, nondirectional cells with a low aspect ratio (AR) responded best to non-Cartesian gratings. These results cannot be fully explained using Gabor linear/energy models of simple and complex receptive fields (RFs) although such models predict some cells to respond equally to Cartesian and non-Cartesian gratings. Cells significantly more responsive to non-Cartesian gratings can be accounted for by CRF selectivity influenced by modulation from the nonclassical receptive field (nCRF). The present study shows that Cartesian/non-Cartesian selectivity is not an emergent property of V4 cells but is present at all levels of early visual processing being subserved by a subset of cells with specific tuning properties.

Strobe rearing reduces direction selectivity in area 17 by altering spatiotemporal receptive-field structure.

Strobe rearing reduces direction selectivity in area 17 by altering spatiotemporal receptive-field structure. J. Neurophysiol. 80: 2991-3004, 1998. Direction selectivity in simple cells of cat area 17 is linked to spatiotemporal (S-T) receptive-field structure. S-T inseparable receptive fields display gradients of response timing across the receptive field that confer a preferred direction of motion. Receptive fields that are not direction selective lack gradients; they are S-T separable, displaying uniform timing across the field. Here we further examine this link using a developmental paradigm that disrupts direction selectivity. Cats were reared from birth to 8 mo of age in 8-Hz stroboscopic illumination. Direction selectivity in simple cells was then measured using gratings drifting at different temporal frequencies (0.25-16 Hz). S-T structure was assessed using stationary bars presented at different receptive-field positions, with bar luminance being modulated sinusoidally at different temporal frequencies. For each cell, plots of response phase versus bar position were fit by lines to characterize S-T inseparability at each temporal frequency. Strobe rearing produced a profound loss of direction selectivity at all temporal frequencies; only 10% of cells were selective compared with 80% in normal cats. The few remaining directional cells were selective over a narrower than normal range of temporal frequencies and exhibited weaker than normal direction selectivity. Importantly, the directional loss was accompanied by a virtual elimination of S-T inseparability. Nearly all cells were S-T separable, like nondirectional cells in normal cats. The loss was clearest in layer 4. Normally, inseparability is greatest there, and it correlates well (r = 0.77) with direction selectivity; strobe rearing reduced inseparability and direction selectivity to very low values. The few remaining directional cells were inseparable. In layer 6 of normal cats, most direction-selective cells are only weakly inseparable, and there is no consistent relationship between the two measures. However, after strobe rearing, even the weak inseparability was eliminated along with direction selectivity. The correlated changes in S-T structure and direction selectivity were confirmed using conventional linear predictions of directional tuning based on responses to counterphasing bars and white noise stimuli. The developmental changes were permanent, being observed up to 12 yr after strobe rearing. The deficits were remarkably specific; strobe rearing did not affect spatial receptive-field structure, orientation selectivity, spatial or temporal frequency tuning, or general responsiveness to visual stimuli. These results provide further support for a critical role of S-T structure in determining direction selectivity in simple cells. Strobe rearing eliminates directional tuning by altering the timing of responses within the receptive field.

Inputs to directionally selective simple cells in macaque striate cortex.

It is clear that the initial analysis of visual motion takes place in the striate cortex, where directionally selective cells are found that respond to local motion in one direction but not in the opposite direction. Widely accepted motion models postulate as inputs to directional units two or more cells whose spatio-temporal receptive fields (RFs) are approximately 90 degrees out of phase (quadrature) in space and in time. Simple cells in macaque striate cortex differ in their spatial phases, but evidence is lacking for the varying time delays required for two inputs to be in temporal quadrature. We examined the space-time RF structure of cells in macaque striate cortex and found two subpopulations of (nondirectional) simple cells, some that show strongly biphasic temporal responses, and others that are weakly biphasic if at all. The temporal impulse responses of these two classes of cells are very close to 90 degrees apart, with the strongly biphasic cells having a shorter latency than the weakly biphasic cells. A principal component analysis of the spatio-temporal RFs of directionally selective simple cells shows that their RFs could be produced by a linear combination of two components; these two components correspond closely in their respective latencies and biphasic characters to those of strongly biphasic and weakly biphasic nondirectional simple cells, respectively. This finding suggests that the motion system might acquire the requisite temporal quadrature by combining inputs from these two classes of nondirectional cells (or from their respective lateral geniculate inputs, which appear to be from magno and parvo lateral geniculate cells, respectively).

Wide-field nondirectional visual units in the pretectum: do they suppress ocular following of saccade-induced visual stimulation

1. Direction-selective neurons in the nucleus of the optic tract (NOT) provide motion signals for controlling ocular following responses. When stimulated at low temporal and high spatial frequencies of motion (slow speeds), these retinal-slip neurons produce directional responses. When stimulated by motion at high temporal and low spatial frequencies (the visual conditions during saccades) the spontaneous activities of the neurons are inhibited by motion in all directions. A second class of neurons in, or near, the NOT have large receptive fields, are nondirectional, and are tuned to detect the same spatial and temporal stimuli that induce nondirectional inhibition in the retinal-slip neurons. We suggest that the nondirectional cells provide an inhibitory input for the retinal-slip neurons and therefore prevent ocular following of the visual displacements that accompany saccades.

Cerebellar neuronal activity related to whole-arm reaching movements in the monkey.

1. Three monkeys were trained to make whole-arm reaching movements from a common central starting position toward eight radially arranged targets disposed at 45 degrees intervals. A sample of 312 cerebellar neurons with proximal-arm receptive fields or discharge related to shoulder or elbow movements was studied in the task. The sample included 69 Purkinje cells, 115 unidentified cortical cells, 65 interpositus neurons, and 63 dentate units. 2. The reaching task was divided into three movement-related epochs: a reaction time, a movement time, and holding over the target. All neurons demonstrated significant changes in discharge during one or more of these three epochs. Almost all of the cells (95%) showed a significant change in activity during the movement, whereas 68-69% of the cells showed significant changes from premovement activity during the reaction time and holding periods. 3. During the combined reaction time-movement period, 231/312 cells were strongly active in the task. Of these, 151 cells (65.4%) demonstrated unimodal directional responses. Sixty-three had a reciprocal relation to movement direction, whereas 88 showed only graded increases or decreases in activity. A further 37 cells (16.0%) were nondirectional, with statistically uniform changes in discharge in all eight directions. The remaining 43 cells (18.6%) showed significant differences in activity for different directions of movement, but their response patterns were not readily classifiable. 4. The proportion of directional versus nondirectional cells was consistent across the four cell populations. However, graded response patterns were more common and reciprocal responses less common among Purkinje and dentate neurons than among unidentified cortical cells and interpositus neurons. 5. The distribution of preferred directions of the population of cerebellar neurons covered all possible movement directions away from the common central starting position in the horizontal plane. When the preferred direction of each cell in the sample population was aligned, the mean direction-related activity of the cerebellar population formed a bell-shaped tuning curve for the activity recorded during both the reaction time and the movement, as well as during the time the arm maintained a fixed posture over the targets. A vector representation also showed that the overall activity of the cerebellar population during normal reaching arm movements generated a signal that varied with movement direction. 6. These results demonstrate that the cerebellum generates a signal that varies with the direction of movement of the proximal arm during normal aimed reaching movements and is consistent with a role in the control of the activity of muscles or muscle groups generating these movements.

Are non-directional simple cells constructed from directional subunits?

Experiments by Schiller et al. have suggested that non-directional edge-specific simple cells are constructed from two directionally selective subunits with opposite preferred direction. This hierarchical notion was based on the fact that the responses of such units to edges moving in opposite directions are spatially displaced with respect to each other. An alternative explanation of the observed response separation is the delay between the responses of the center and surround mechanisms at the retinal level. Measurements of the response separation as a function of stimulus speed support this explanation and argues against the hierarchical notion of Schiller et al.

Suppressive regions in the visual receptive fields of single cells of the pigeon's optic tectum.

Single unit extracellular recordings were obtained from non-directional and from directionally selective cells in the pigeon's optic tectum. Non-directional cells were classified according to their excitatory dynamic profiles into three classes. Class A: cells showing spatially superimposed light and dark regions in their fields. Class B: cells showing spatially separated light and dark regions in their fields. Class C: cells which responded exclusively to one sign of contrast. Most of the cells in our sample showed a suppressive region outside the excitatory area from where moving stimuli were able to reduce the units' "spontaneous" background firing. Suppressive regions were found in directionally selective as well as in non-directional cells, regardless of their dynamic excitatory profiles, with the exception of Class C cells. Evidence of spatial overlapping between the excitatory and the suppressive region was obtained with both moving and flashed stimuli. Furthermore, suppressive antagonistic effects were observed in Class B cells.

Non-directional and directional ganglion cells in the pigeon retina

Intraretinal recordings were taken from ganglion cells in the pigeon retina, and histograms were taken from non-directional cells in the presence of baseline spike counts, responding to stimuli moving back and forth through their receptive fields. The profiles revealed in this way differ in on-off, on-centre and off-centre cells. The majority of non-directional cells do not give evidence for inhibitory surrounds activated by the moving stimulus. A minority do show inhibitory surrounds, which can delete driven spikes.

Single-neuron responses to moving sine-wave gratings in the pigeon optic tectum

The responses of single cells in the superficial layers of the pigeon optic tectum to moving sine-wave gratings were analysed quantitatively. From these responses, cells could be identified as modulated or non-modulated. About 80% of the units tested were found to be spatial frequency dependent. Some cells have spatial frequency tuning curves with both high- and low-frequency response cutoff: others have only a high-frequency cutoff. Directional and nondirectional cells showed no differences in responses to gratings. No correlation was found between the optimal spatial frequency response and either the size of the receptive field or retinal eccentricity. Responses could be greatly affected by contrast. The inhibitory surround has no effect upon the specification of the cell spatial selectivity. The higher resolution value for square-wave gratings at 60% contrast was 7 c/deg. These findings suggest that tectal cells in pigeon may be able to code spatial information.

Intracellular responses from cells of the medulla of the fly, Calliphora erythrocephala.

1. Intracellular recordings were made from cells in medullae of immobilized, intact flies Calliphora erythrocephala. Stimuli were moving gratings or small spots projected onto translucent hemispheres before the fly.--2. Responses to stationary flashes included tonic and phasic slow potentials only. Sustaining and On/Off discharges were recorded from cells silent in the dark. Sustaining, dimming, On/Off, +On-Off, and-On/-Off discharges were recorded from cells spontaneous in the dark (Fig. 1, 2, and 3).--3. Some cells were relatively sensitive to 3 log unit changes in flash intensities; others were insensitive (Fig. 4).--4. Receptive fields of a few cells tested were small-field ipsilateral monocular, large-field ipsilateral monocular, or large-field binocular.--5. A number of types of nondirectional cells were found. Some gave stronger discharges to movement than to stationary flashes (Fig. 5).--6. Directionally-selective cells were generally spontaneous. Some simply fired faster in the preferred direction. Others (Fig. 6) had inhibition in the null diriction with or without hyperpolarizations.--7. Possibly-new nondirectional cells were found that were inhibited by changes of direction of movement (Fig. 7)--8. A number of cells were stained with Procion yellow, using high voltage pulses. Double stainings sometimes occurred (Fig. 8).

Binocular interaction in the cat's superior colliculus.

1. Binocularly driven neurones with small receptive fields near the area centralis were recorded in the cat's superior colliculus. 2. Binocular interaction was tested by stimulating both eyes simultaneously with a single moving stimulus at various retinal disparities. 3. Collicular cells in general showed strong summation or even facilitation when the images of the stimulus were in exact correspondence on the receptive fields, sometimes with occlusion when they were out of register. The range of retinal disparity over which there was additive interaction could be as little as 1 or 2 deg, almost as narrow as for the most precisely tuned neurones in the visual cortex. Even cells with large receptive fields sometimes showed a narrow range of binocular interaction. 4. Non-directional cells generally exhibited weaker summation and broader disparity selectivity than did direction-selective cells. 5. Some neurones with virtually no response to a stimulus in one of the eyes can exhibit marked binocular interaction. Other apparently monocular cells show little or no binocular interaction. 6. The disparity of the centres of the receptive fields was measured after correcting for small eye movements, which were assessed by two different techniques. For 132 cells the measured distribution of horizontal disparity (range 4.5 deg; S.D. 0.93 deg) was significantly broader than that of vertical disparity (range 2.2 deg; S.D. 0.52 deg). Sources of error in these measurements are considered. 7. The results are discussed in relation to the known connexions between visual cortex and superior colliculus and the possible role of the latter in the regulation of eye movements.