scholarly journals Excitatory and inhibitory intracortical circuits for orientation and direction selectivity

2019 ◽  
Author(s):  
L. Federico Rossi ◽  
Kenneth D. Harris ◽  
Matteo Carandini
Keyword(s):  
Functional Properties ◽  
Functional Organization ◽  
Direction Selectivity ◽  
Orientation Selectivity ◽  
Preferred Orientation ◽  
Inhibitory Input ◽  
Postsynaptic Neuron ◽  
Preferred Direction ◽  
Intracortical Circuits ◽  
Presynaptic Neurons

The computations performed by a neuron arise from the functional properties of the circuits providing its synaptic inputs. A prime example of these computations is the selectivity of primary visual cortex (V1) for orientation and motion direction. V1 neurons in layer 2/3 (L2/3) receive input mostly from intracortical circuits1, which involve excitation2-9 and inhibition10-12. To understand how an L2/3 neuron achieves its selectivity, therefore, one must characterize the functional organization of both its excitatory and inhibitory presynaptic ensembles. Here we establish this organization, and show how it predicts orientation selectivity and reveals a new cortical circuit for direction selectivity. We identified the presynaptic partners of pyramidal neurons in mouse V1 through rabies monosynaptic tracing1,13, and imaged the functional properties of the postsynaptic neuron and of its presynaptic ensemble. Excitatory presynaptic neurons were predominantly tuned to the postsynaptic neuron’s preferred orientation. Excitation and inhibition described an inverted Mexican hat, with inhibitory presynaptic neurons densest near the postsynaptic neuron and excitatory ones distributed more distally. Excitation and inhibition also differed in laminar origin: inhibitory presynaptic neurons concentrated in L2/3 while excitatory ones dominated in L4. The distribution of excitatory neurons in visual space was coaxial with the postsynaptic neuron’s preferred orientation and lay upstream of the neuron’s preferred direction. Inhibitory presynaptic neurons, instead, clustered more symmetrically around the postsynaptic neuron and favoured locations downstream of its preferred direction. These results demonstrate that L2/3 neurons obtain orientation selectivity from co-tuned neurons in L4 and beyond, and enhance it by contrasting an elongated excitatory input with a concentric inhibitory input. Moreover, L2/3 neurons can obtain direction selectivity through visually offset14 excitation and inhibition. These circuit motifs resemble those seen in the thalamocortical pathway15-20 and in direction selective cells in the retina21,22, suggesting that they are canonical across brain regions.

GABA-induced inactivation of functionally characterized sites in cat striate cortex: Effects on orientation tuning and direction selectivity

1997 ◽  
Vol 14 (1) ◽  
pp. 141-158 ◽  
Author(s):  
John M. Crook ◽  
Zoltan F. Kisvárday ◽  
Ulf T. Eysel
Keyword(s):  
Opposite Direction ◽  
Striate Cortex ◽  
Single Cells ◽  
Direction Selectivity ◽  
Orientation Tuning ◽  
Inhibitory Input ◽  
Horizontal Distance ◽  
Area 17 ◽  
Preferred Direction ◽  
Direction Preference

AbstractMicroiontophoresis of γ-aminobutyric acid (GABA) was used to reversibly inactivate small sites of defined orientation/direction specificity in layers II-IV of cat area 17 while single cells were recorded in the same area at a horizontal distance of ~350–700 jam. We compared the effect of inactivating iso-orientation sites (where orientation preference was within 22.5 deg) and cross-orientation sites (where it differed by 45–90 deg) on orientation tuning and directionality. The influence of iso-orientation inactivation was tested in 33 cells, seven of which were subjected to alternate inactivation of two iso-orientation sites with opposite direction preference. Of the resulting 40 inactivations, only two (5%) caused significant changes in orientation tuning, whereas 26 (65%) elicited effects on directionality: namely, an increase or a decrease in response to a cell's preferred direction when its direction preference was the same as that at an inactivation site, and an increase in response to a cell's nonpreferred direction when its direction preference was opposite that at an inactivation site. It is argued that the decreases in response to the preferred direction reflected a reduction in the strength of intracortical iso-orientation excitatory connections, while the increases in response were due to the loss of iso-orientation inhibition. Of 35 cells subjected to cross-orientation inactivation, only six (17%) showed an effect on directionality, whereas 21 (60%) showed significant broadening of orientation tuning, with an increase in mean tuning width at half-height of 126%. The effects on orientation tuning were due to increases in response to nonoptimal orientations. Changes in directionality also resulted from increased responses (to preferred or nonpreferred directions) and were always accompanied by broadening of tuning. Thus, the effects of cross-orientation inactivation were presumably due to the loss of a cross-orientation inhibitory input that contributes mainly to orientation tuning by suppressing responses to nonoptimal orientations. Differential effects of iso-orientation and cross-orientation inactivation could be elicited in the same cell or in different cells from the same inactivation site. The results suggest the involvement of three different intracortical processes in the generation of orientation tuning and direction selectivity in area 17: (1) suppression of responses to nonoptimal orientations and directions as a result of cross-orientation inhibition and iso-orientation inhibition between cells with opposite direction preferences; (2) amplification of responses to optimal stimuli via iso-orientation excitatory connections; and (3) regulation of cortical amplification via iso-orientation inhibition.

Direction and orientation selectivity of neurons in visual area MT of the macaque

1984 ◽  
Vol 52 (6) ◽  
pp. 1106-1130 ◽  
Author(s):  
T. D. Albright
Keyword(s):  
Direction Selectivity ◽  
Orientation Selectivity ◽  
Orientation Tuning ◽  
Area Mt ◽  
Mt Neurons ◽  
V1 Neurons ◽  
Moving Stimuli ◽  
Preferred Direction ◽  
Visual Area Mt ◽  
Direction Tuning

We recorded from single neurons in the middle temporal visual area (MT) of the macaque monkey and studied their direction and orientation selectivity. We also recorded from single striate cortex (V1) neurons in order to make direct comparisons with our observations in area MT. All animals were immobilized and anesthetized with nitrous oxide. Direction selectivity of 110 MT neurons was studied with three types of moving stimuli: slits, single spots, and random-dot fields. All of the MT neurons were found to be directionally selective using one or more of these stimuli. MT neurons exhibited a broad range of direction-tuning bandwidths to all stimuli (minimum = 32 degrees, maximum = 186 degrees, mean = 95 degrees). On average, responses were strongly unidirectional and of similar magnitude for all three stimulus types. Orientation selectivity of 89 MT neurons was studied with stationary flashed slits. Eighty-three percent were found to be orientation selective. Overall, orientation-tuning bandwidths were significantly narrower (mean = 64 degrees) than direction-tuning bandwidths for moving stimuli. Moreover, responses to stationary-oriented stimuli were generally smaller than those to moving stimuli. Direction selectivity of 55 V1 neurons was studied with moving slits; orientation selectivity of 52 V1 neurons was studied with stationary flashed slits. In V1, compared with MT, direction-tuning bandwidths were narrower (mean = 68 degrees). Moreover, V1 responses to moving stimuli were weaker, and bidirectional tuning was more common. The mean orientation-tuning bandwidth in V1 was also significantly narrower than that in MT (mean = 52 degrees), but the responses to stationary-oriented stimuli were of similar magnitude in the two areas. We examined the relationship between optimal direction and optimal orientation for MT neurons and found that 61% had an orientation preference nearly perpendicular to the preferred direction of motion, as is the case for all V1 neurons. However, another 29% of MT neurons had an orientation preference roughly parallel to the preferred direction. These observations, when considered together with recent reports claiming sensitivity of some MT neurons to moving visual patterns (39), suggest specific neural mechanisms underlying pattern-motion sensitivity in area MT. These results support the notion that area MT represents a further specialization over area V1 for stimulus motion processing. Furthermore, the marked similarities between direction and orientation tuning in area MT in macaque and owl monkey support the suggestion that these areas are homologues.

Organization of orientation and direction selectivity in areas 17 and 18 of cat cerebral cortex

1987 ◽  
Vol 58 (4) ◽  
pp. 676-699 ◽  
Author(s):  
N. E. Berman ◽  
M. E. Wilkes ◽  
B. R. Payne
Keyword(s):  
Receptive Fields ◽  
Direction Selectivity ◽  
Preferred Orientation ◽  
Wide Field ◽  
Area 17 ◽  
Stimulus Motion ◽  
Area 18 ◽  
Preferred Direction ◽  
Area Centralis ◽  
Areas 17 And 18

1. The organization of subunits and sequences subserving preferred stimulus orientation and preferred direction of stimulus motion in cat cerebral cortical areas 17 and 18 was determined by making vertical, tangential, and oblique microelectrode penetrations into those areas. 2. Quantitative measurements of direction selectivity indicated that not all shades of direction selectivity are equally represented in area 17. Peaks in the distribution of direction indices may correspond to the bidirectional, direction biased, and direction selective categories used in qualitative studies. 3. The relationship between preferred direction and location in the visual field was examined for units with receptive fields centered more than 15 degrees from the area centralis. Simple cells had orientation preferences that tended to be parallel to radii extending out from the area centralis. Wide-field complex cells had orientation preferences that tended to be parallel to concentric circles centered on the area centralis; the direction preferences of this group were biased toward motion away from the area centralis. 4. Unit pairs separated by 200 microns or less were 4.2 times as likely to have the same preferred direction as to have opposite preferred directions, indicating that, on average, strings of five neurons have similar direction preferences. 5. Tracks in area 18 showed a similar pattern to those in area 17. 6. In the vertical tracks in area 17 a small proportion (12%) of the units recorded in infragranular layers had preferred orientations that deviated 30 degrees or more from the first unit recorded in the same column. The presence of these cells most likely reflects the relative crowding of columns in infragranular layers, which occurs at the crown of the lateral gyrus. Columns with such large jumps in preferred orientation were not observed in area 18, which occupies a relatively flat region of cortex. 7. In both areas 17 and 18 direction preference in vertical tracks usually reversed at least once, either between supra- and infragranular layers or within infragranular layers. Along these same tracks, orientation preference usually did not change. 8. In tangential tracks, preferred direction and orientation preferences changed together in small increments. Occasionally a large jump in preferred direction would occur with only a small change in preferred orientation. These large jumps were considered to mark the boundaries of the direction sequences. Most frequently these boundaries were separated by 400-600 microns. This value is approximately half the size of a complete set of orientation preferences (700-1,200 microns).(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals Orientation selectivity in the visual cortex of the nine-banded armadillo

2017 ◽  
Vol 117 (3) ◽  
pp. 1395-1406 ◽  
Author(s):  
Benjamin Scholl ◽  
Johnathan Rylee ◽  
Jeffrey J. Luci ◽  
Nicholas J. Priebe ◽  
Jeffrey Padberg
Keyword(s):  
Visual Cortex ◽  
Functional Properties ◽  
Primary Visual Cortex ◽  
Functional Organization ◽  
Orientation Selectivity ◽  
Small Subset ◽  
Motion Direction ◽  
V1 Neurons ◽  
Wide Range ◽  
Degree Of Orientation

Orientation selectivity in primary visual cortex (V1) has been proposed to reflect a canonical computation performed by the neocortical circuitry. Although orientation selectivity has been reported in all mammals examined to date, the degree of selectivity and the functional organization of selectivity vary across mammalian clades. The differences in degree of orientation selectivity are large, from reports in marsupials that only a small subset of neurons are selective to studies in carnivores, in which it is rare to find a neuron lacking selectivity. Furthermore, the functional organization in cortex varies in that the primate and carnivore V1 is characterized by an organization in which nearby neurons share orientation preference while other mammals such as rodents and lagomorphs either lack or have only extremely weak clustering. To gain insight into the evolutionary emergence of orientation selectivity, we examined the nine-banded armadillo, a species within the early placental clade Xenarthra. Here we use a combination of neuroimaging, histological, and electrophysiological methods to identify the retinofugal pathways, locate V1, and for the first time examine the functional properties of V1 neurons in the armadillo ( Dasypus novemcinctus) V1. Individual neurons were strongly sensitive to the orientation and often the direction of drifting gratings. We uncovered a wide range of orientation preferences but found a bias for horizontal gratings. The presence of strong orientation selectivity in armadillos suggests that the circuitry responsible for this computation is common to all placental mammals.NEW & NOTEWORTHY The current study shows that armadillo primary visual cortex (V1) neurons share the signature properties of V1 neurons of primates, carnivorans, and rodents. Furthermore, these neurons exhibit a degree of selectivity for stimulus orientation and motion direction similar to that found in primate V1. Our findings in armadillo visual cortex suggest that the functional properties of V1 neurons emerged early in the mammalian lineage, near the time of the divergence of marsupials.

scholarly journals The functional organization of excitation and inhibition in the dendritic arbors of retinal direction-selective ganglion cells

2019 ◽  
Author(s):  
Varsha Jain ◽  
Benjamin L. Murphy-Baum ◽  
Geoff deRosenroll ◽  
Santhosh Sethuramanujam ◽  
Mike Delsey ◽  
...  
Keyword(s):  
Functional Organization ◽  
Ganglion Cells ◽  
Dendritic Tree ◽  
Amacrine Cells ◽  
Direction Selectivity ◽  
Inhibitory Input ◽  
Processing Scheme ◽  
Fine Grained ◽  
Cell Ablation ◽  
Starburst Amacrine Cells

SUMMARYRecent studies indicate that the precise timing and location of excitation and inhibition (E/I) within active dendritic trees can significantly impact neuronal function. How excitatory and inhibitory inputs are functionally organized at the subcellular level in intact circuits remains unclear. To address this issue, we took advantage of the retinal direction-selective ganglion cell circuit, in which directionally tuned inhibitory GABAergic input arising from starburst amacrine cells shape direction-selective dendritic responses. We combined two-photon Ca2+ imaging with genetic, pharmacological, and single-cell ablation methods to examine local E/I. We demonstrate that when active dendritic conductances are blocked, direction selectivity emerges semi-independently within unusually small dendritic segments (<10 µm). Impressively, the direction encoded by each segment is relatively homogenous throughout the ganglion cell’s dendritic tree. Together the results demonstrate a precise subcellular functional organization of excitatory and inhibitory input, which suggests that the parallel processing scheme proposed for direction encoding could be more fine-grained than previously envisioned.

scholarly journals Modeling simple-cell direction selectivity with normalized, half-squared, linear operators

1993 ◽  
Vol 70 (5) ◽  
pp. 1885-1898 ◽  
Author(s):  
D. J. Heeger
Keyword(s):  
Linear Prediction ◽  
Direction Selectivity ◽  
Linear Operators ◽  
Simple Cell ◽  
Physiological Data ◽  
Simple Cells ◽  
Cell Responses ◽  
Preferred Direction ◽  
Model Cell ◽  
Actual Response

1. A longstanding view of simple cells is that they sum their inputs linearly. However, the linear model falls short of a complete account of simple-cell direction selectivity. We have developed a nonlinear model of simple-cell responses (hereafter referred to as the normalization model) to explain a larger body of physiological data. 2. The normalization model consists of an underlying linear stage along with two additional nonlinear stages. The first is a half-squaring nonlinearity; half-squaring is half-wave rectification followed by squaring. The second is a divisive normalization non-linearity in which each model cell is suppressed by the pooled activity of a large number of cells. 3. By comparing responses with counterphase (flickering) gratings and drifting gratings, researchers have demonstrated that there is a nonlinear contribution to simple-cell responses. Specifically they found 1) that the linear prediction from counterphase grating responses underestimates a direction index computed from drifting grating responses, 2) that the linear prediction correctly estimates responses to gratings drifting in the preferred direction, and 3) that the linear prediction overestimates responses to gratings drifting in the nonpreferred direction. 4. We have simulated model cell responses and derived mathematical expressions to demonstrate that the normalization model accounts for this empirical data. Specifically the model behaves as follows. 1) The linear prediction from counterphase data underestimates the direction index computed from drifting grating responses. 2) The linear prediction from counterphase data overestimates the response to gratings drifting in the nonpreferred direction. The discrepancy between the linear prediction and the actual response is greater when using higher contrast stimuli. 3) For an appropriate choice of contrast, the linear prediction from counterphase data correctly estimates the response to gratings drifting in the preferred direction. For higher contrasts the linear prediction overestimates the actual response, and for lower contrasts the linear prediction underestimates the actual response. 5. In addition, the normalization model is qualitatively consistent with data on the dynamics of simple-cell responses. Tolhurst et al. found that simple cells respond with an initial transient burst of activity when a stimulus first appears. The normalization model behaves similarly; it takes some time after a stimulus first appears before the model cells are fully normalized. We derived the dynamics of the model and found that the transient burst of activity in model cells depends in a particular way on stimulus contrast. The burst is short for high-contrast stimuli and longer for low-contrast stimuli.(ABSTRACT TRUNCATED AT 400 WORDS)

Directional selectivity and spatiotemporal structure of receptive fields of simple cells in cat striate cortex

1991 ◽  
Vol 66 (2) ◽  
pp. 505-529 ◽  
Author(s):  
R. C. Reid ◽  
R. E. Soodak ◽  
R. M. Shapley
Keyword(s):  
Time Course ◽  
Linear Prediction ◽  
Striate Cortex ◽  
Receptive Fields ◽  
Quantitative Measure ◽  
Direction Selectivity ◽  
Simple Cells ◽  
Preferred Direction ◽  
Orientation Contrast ◽  
Cat Striate Cortex

1. Simple cells in cat striate cortex were studied with a number of stimulation paradigms to explore the extent to which linear mechanisms determine direction selectivity. For each paradigm, our aim was to predict the selectivity for the direction of moving stimuli given only the responses to stationary stimuli. We have found that the prediction robustly determines the direction and magnitude of the preferred response but overestimates the nonpreferred response. 2. The main paradigm consisted of comparing the responses of simple cells to contrast reversal sinusoidal gratings with their responses to drifting gratings (of the same orientation, contrast, and spatial and temporal frequencies) in both directions of motion. Although it is known that simple cells display spatiotemporally inseparable responses to contrast reversal gratings, this spatiotemporal inseparability is demonstrated here to predict a certain amount of direction selectivity under the assumption that simple cells sum their inputs linearly. 3. The linear prediction of the directional index (DI), a quantitative measure of the degree of direction selectivity, was compared with the measured DI obtained from the responses to drifting gratings. The median value of the ratio of the two was 0.30, indicating that there is a significant nonlinear component to direction selectivity. 4. The absolute magnitudes of the responses to gratings moving in both directions of motion were compared with the linear predictions as well. Whereas the preferred direction response showed only a slight amount of facilitation compared with the linear prediction, there was a significant amount of nonlinear suppression in the nonpreferred direction. 5. Spatiotemporal inseparability was demonstrated also with stationary temporally modulated bars. The time course of response to these bars was different for different positions in the receptive field. The degree of spatiotemporal inseparability measured with sinusoidally modulated bars agreed quantitatively with that measured in experiments with stationary gratings. 6. A linear prediction of the responses to drifting luminance borders was compared with the actual responses. As with the grating experiments, the prediction was qualitatively accurate, giving the correct preferred direction but underestimating the magnitude of direction selectivity observed.(ABSTRACT TRUNCATED AT 400 WORDS)

Functional Role of the Left Ventral Occipito-Temporal Cortex in Reading

2013 ◽  
pp. 192-200
Author(s):  
Geqi Qi ◽  
Jinglong Wu
Keyword(s):  
Functional Properties ◽  
Functional Role ◽  
Word Processing ◽  
Functional Organization ◽  
Temporal Cortex ◽  
Visual Word ◽  
Word Form ◽  
Considerable Debate ◽  
Two Sides

The sensitivity of the left ventral occipito-temporal (vOT) cortex to visual word processing has triggered a considerable debate about the functional role of this region in reading. The debate rests largely on the issue whether this particular region is specifically dedicated to reading and the extraction of invariant visual word form. A lot of studies have been conducted to provide evidences supporting or against the functional specialization of this region. However, the trend is showing that the different functional properties proposed by the two kinds of view are not in conflict with each other, but instead show different sides of the same fact. Here, the authors focus on two questions: firstly, where do the two views conflict, and secondly, how do they fit with each other on a larger framework of functional organization in object vision pathway? This review evaluates findings from the two sides of the debate for a broader understanding of the functional role of the left vOT cortex.

scholarly journals Weighting neurons by selectivity produces near-optimal population codes

2019 ◽  
Vol 121 (5) ◽  
pp. 1924-1937
Author(s):  
Elizabeth Zavitz ◽  
Nicholas S. C. Price
Keyword(s):  
A Priori ◽  
Maximum Level ◽  
Optimization Methods ◽  
Neuronal Population ◽  
Direction Selectivity ◽  
Motion Direction ◽  
Temporal Area ◽  
Linear Discriminant ◽  
Preferred Direction

Perception is produced by “reading out” the representation of a sensory stimulus contained in the activity of a population of neurons. To examine experimentally how populations code information, a common approach is to decode a linearly weighted sum of the neurons’ spike counts. This approach is popular because of the biological plausibility of weighted, nonlinear integration. For neurons recorded in vivo, weights are highly variable when derived through optimization methods, but it is unclear how the variability affects decoding performance in practice. To address this, we recorded from neurons in the middle temporal area (MT) of anesthetized marmosets ( Callithrix jacchus) viewing stimuli comprising a sheet of dots that moved coherently in 1 of 12 different directions. We found that high peak response and direction selectivity both predicted that a neuron would be weighted more highly in an optimized decoding model. Although learned weights differed markedly from weights chosen according to a priori rules based on a neuron’s tuning profile, decoding performance was only marginally better for the learned weights. In the models with a priori rules, selectivity is the best predictor of weighting, and defining weights according to a neuron’s preferred direction and selectivity improves decoding performance to very near the maximum level possible, as defined by the learned weights. NEW & NOTEWORTHY We examined which aspects of a neuron’s tuning account for its contribution to sensory coding. Strongly direction-selective neurons are weighted most highly by optimal decoders trained to discriminate motion direction. Models with predefined decoding weights demonstrate that this weighting scheme causally improved direction representation by a neuronal population. Optimizing decoders (using a generalized linear model or Fisher’s linear discriminant) led to only marginally better performance than decoders based purely on a neuron’s preferred direction and selectivity.

Sign in / Sign up

Export Citation Format

Share Document