scholarly journals A theory of direction selectivity for macaque primary visual cortex

2021 ◽  
Vol 118 (32) ◽  
pp. e2105062118
Author(s):  
Logan Chariker ◽  
Robert Shapley ◽  
Michael Hawken ◽  
Lai-Sang Young
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Cortical Neurons ◽  
Temporal Frequency ◽  
Cortical Cell ◽  
Direction Selectivity ◽  
Complete Analysis ◽  
Visual Response ◽  
Response Dynamics ◽  
Preferred Direction

This paper offers a theory for the origin of direction selectivity (DS) in the macaque primary visual cortex, V1. DS is essential for the perception of motion and control of pursuit eye movements. In the macaque visual pathway, neurons with DS first appear in V1, in the Simple cell population of the Magnocellular input layer 4Cα. The lateral geniculate nucleus (LGN) cells that project to these cortical neurons, however, are not direction selective. We hypothesize that DS is initiated in feed-forward LGN input, in the summed responses of LGN cells afferent to a cortical cell, and it is achieved through the interplay of 1) different visual response dynamics of ON and OFF LGN cells and 2) the wiring of ON and OFF LGN neurons to cortex. We identify specific temporal differences in the ON/OFF pathways that, together with item 2, produce distinct response time courses in separated subregions; analysis and simulations confirm the efficacy of the mechanisms proposed. To constrain the theory, we present data on Simple cells in layer 4Cα in response to drifting gratings. About half of the cells were found to have high DS, and the DS was broadband in spatial and temporal frequency (SF and TF). The proposed theory includes a complete analysis of how stimulus features such as SF and TF interact with ON/OFF dynamics and LGN-to-cortex wiring to determine the preferred direction and magnitude of DS.

scholarly journals A theory of direction selectivity for Macaque primary visual cortex

2021 ◽  
Author(s):  
Logan Chariker ◽  
Robert Shapley ◽  
Michael Hawken ◽  
Lai-Sang Young
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Cortical Neurons ◽  
Temporal Frequency ◽  
Broad Band ◽  
Cortical Cell ◽  
Direction Selectivity ◽  
Complete Analysis ◽  
Visual Response ◽  
Response Dynamics

This paper offers a new theory for the origin of direction selectivity in the Macaque primary visual cortex, V1. Direction selectivity (DS) is essential for the perception of motion and control of pursuit eye movements. In the Macaque visual pathway, DS neurons first appear in V1, in the Simple cell population of the Magnocellular input layer 4Ca. The LGN cells that project to these cortical neurons, however, are not direction-selective. We hypothesize that DS is initiated in feedforward LGN input, in the summed responses of LGN cells afferent to a cortical cell, and it is achieved through the interplay of (a) different visual response dynamics of ON and OFF LGN cells, and (b) the wiring of ON and OFF LGN neurons to cortex. We identify specific temporal differences in the ON/OFF pathways that together with (b) produce distinct response time-courses in separated subregions; analysis and simulations confirm the efficacy of the mechanisms proposed. To constrain the theory, we present data on Simple cells in layer 4Ca in response to drifting gratings. About half of the cells were found to have high DS, and the DS was broad-band in spatial and temporal frequency (SF and TF). The proposed theory includes a complete analysis of how stimulus features such as SF and TF interact with ON/OFF dynamics and LGN-to-cortex wiring to determine the preferred direction and magnitude of DS.

scholarly journals Orientation Tuning, But Not Direction Selectivity, Is Invariant to Temporal Frequency in Primary Visual Cortex

2005 ◽  
Vol 94 (2) ◽  
pp. 1336-1345 ◽  
Author(s):  
Bartlett D. Moore ◽  
Henry J. Alitto ◽  
W. Martin Usrey
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Visual Stimulus ◽  
Visual Processing ◽  
Cortical Neurons ◽  
Temporal Frequency ◽  
Direction Selectivity ◽  
Orientation Tuning ◽  
Orientation Contrast ◽  
Wide Range

The activity of neurons in primary visual cortex is influenced by the orientation, contrast, and temporal frequency of a visual stimulus. This raises the question of how these stimulus properties interact to shape neuronal responses. While past studies have shown that the bandwidth of orientation tuning is invariant to stimulus contrast, the influence of temporal frequency on orientation-tuning bandwidth is unknown. Here, we investigate the influence of temporal frequency on orientation tuning and direction selectivity in area 17 of ferret visual cortex. For both simple cells and complex cells, measures of orientation-tuning bandwidth (half-width at half-maximum response) are ∼20–25° across a wide range of temporal frequencies. Thus cortical neurons display temporal-frequency invariant orientation tuning. In contrast, direction selectivity is typically reduced, and occasionally reverses, at nonpreferred temporal frequencies. These results show that the mechanisms contributing to the generation of orientation tuning and direction selectivity are differentially affected by the temporal frequency of a visual stimulus and support the notion that stability of orientation tuning is an important aspect of visual processing.

scholarly journals Influence of Contrast on Orientation and Temporal Frequency Tuning in Ferret Primary Visual Cortex

2004 ◽  
Vol 91 (6) ◽  
pp. 2797-2808 ◽  
Author(s):  
Henry J. Alitto ◽  
W. Martin Usrey
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Cortical Neurons ◽  
Frequency Tuning ◽  
Temporal Frequency ◽  
Orientation Tuning ◽  
Visual Response ◽  
Stimulus Contrast ◽  
Tuning Curves ◽  
Simple And Complex Cells

Neurons in primary visual cortex are highly sensitive to the contrast, orientation, and temporal frequency of a visual stimulus. These three stimulus properties can be varied independently of one another, raising the question of how they interact to influence neuronal responses. We recorded from individual neurons in ferret primary visual cortex to determine the influence of stimulus contrast on orientation tuning, temporal-frequency tuning, and latency to visual response. Results show that orientation-tuning bandwidth is not affected by contrast level. Thus neurons in ferret visual cortex display contrast-invariant orientation tuning. Stimulus contrast does, however, influence the structure of orientation-tuning curves as measures of circular variance vary inversely with contrast for both simple and complex cells. This change in circular variance depends, in part, on a contrast-dependent change in the ratio of null to preferred orientation responses. Stimulus contrast also has an influence on the temporal-frequency tuning of cortical neurons. Both simple and complex cells display a contrast-dependent rightward shift in their temporal frequency-tuning curves that results in an increase in the highest temporal frequency needed to produce a half-maximum response (TF50). Results show that the degree of the contrast-dependent increase in TF50 is similar for cortical neurons and neurons in the lateral geniculate nucleus (LGN) and indicate that subcortical mechanisms likely play a major role in establishing the degree of effect displayed by downstream neurons. Finally, results show that LGN and cortical neurons experience a contrast-dependent phase advance in their visual response. This phase advance is most pronounced for cortical neurons indicating a role for both subcortical and cortical mechanisms.

Mechanisms underlying direction selectivity of neurons in the primary visual cortex of the macaque

1995 ◽  
Vol 74 (4) ◽  
pp. 1382-1394 ◽  
Author(s):  
H. Sato ◽  
N. Katsuyama ◽  
H. Tamura ◽  
Y. Hata ◽  
T. Tsumoto
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Threshold Level ◽  
Intracortical Inhibition ◽  
Direction Selectivity ◽  
Gamma Aminobutyric Acid ◽  
Visual Responses ◽  
Preferred Direction ◽  
Control Response ◽  
Layer Vi

1. We studied the effects of blocking intracortical inhibition by microiontophoretic administration of bicuculline methiodide (BMI), a selective antagonist for gamma-aminobutyric acid-A receptors, on direction sensitivity of 103 neurons in the primary visual cortex (VI) of anesthetized and paralyzed monkeys. 2. The direction selectivity index (DSI) of each cell was calculated for the control response and response during the BMI administration at the optimal stimulus orientation to assess the directionality of an individual cell. 3. The averaged direction tuning of visual responses of cells was sharp in layers IVa and IVb, moderate in both interblob and blob regions of layer II/III and layers V and VI, and poor in layers IVc alpha and IVc beta. 4. Iontophoretic administration of BMI uncovered or facilitated responses to stimuli moving in the nonpreferred direction, and reduced DSIs of cells to a varying extent in all the layers except layer VI. Responses to stimuli moving in the preferred direction were also facilitated so that a slight bias of response toward the originally preferred direction remained during BMI administration in most cells. 5. Most of the cells in layers II/III (both blobs and interblobs) and IVb that receive inputs from layers IVc alpha and IVc beta showed a clear reduction of direction selectivity during BMI administration. This result suggests that intracortical inhibition plays an important role in the elaboration of direction selectivity at the second stage of information processing in VI. 6. The direction selectivity of cells in layer VI was most resistant to the effects of BMI, suggesting that it is dependent on excitatory inputs that are already direction selective, even though the sample size of this layer was small. 7. In direction-selective cells outside layer VI, responses to a stimulus moving in the preferred direction were enhanced in a way that was linearly related with those in the nonpreferred direction as the BMI dose was increased. This suggests that various amounts of inhibition interact linearly with directionally biased excitatory inputs to raise the firing threshold to various levels so as to produce various degrees of directionality. 8. These results suggest that, in most of the directionally sensitive cells except for those in layer VI, there are excitatory inputs which are bidirectional but slightly biased to one direction, and that the intracortical inhibition raises a threshold level of responses to excitatory inputs so that the response become direction selective.

Temporal-frequency tuning of direction selectivity in cat visual cortex

1992 ◽  
Vol 8 (4) ◽  
pp. 365-372 ◽  
Author(s):  
Alan B. Saul ◽  
Allen L. Humphrey
Keyword(s):  
Visual Cortex ◽  
Frequency Tuning ◽  
Temporal Frequency ◽  
Direction Selectivity ◽  
Half Cycle ◽  
Low Frequencies ◽  
Preferred Direction ◽  
Cat Visual Cortex ◽  
Cortical Responses ◽  
Areas 17 And 18

AbstractResponses of 71 cells in areas 17 and 18 of the cat visual cortex were recorded extracellularly while stimulating with gratings drifting in each direction across the receptive field at a series of temporal frequencies. Direction selectivity was most prominent at temporal frequencies of 1–2 Hz. In about 20% of the total population, the response in the nonpreferred direction increased at temporal frequencies of around 4 Hz and direction selectivity was diminished or lost. In a few cells the preferred direction reversed.One consequence of this behavior was a tendency for the preferred direction to have lower optimal temporal frequencies than the nonpreferred direction. Across the population, the preferred direction was tuned almost an octave lower. In spite of this, temporal resolution was similar in the two directions. It appeared that responses in the nonpreferred direction were suppressed at low frequencies, then recovered at higher frequencies.This phenomenon might reflect the convergence in visual cortex of lagged and nonlagged inputs from the lateral geniculate nucleus. These afferents fire about a quarter-cycle apart (i.e. are in temporal quadrature) at low temporal frequencies, but their phase difference increases to a half-cycle by about 4 Hz. Such timing differences could underlie the prevalence of direction-selective cortical responses at 1 and 2 Hz and the loss of direction selectivity in many cells by 4 or 8 Hz.

Complex motion selectivity in PMLS cortex following early lesions of primary visual cortex in the cat

2007 ◽  
Vol 24 (1) ◽  
pp. 53-64 ◽  
Author(s):  
B.G. OUELLETTE ◽  
K. MINVILLE ◽  
D. BOIRE ◽  
M. PTITO ◽  
C. CASANOVA
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Visual Motion ◽  
Neuronal Response ◽  
Temporal Frequency ◽  
Limited Range ◽  
Direction Selectivity ◽  
Motion Processing ◽  
Complex Motion ◽  
Visual Motion Cues

In the cat, the analysis of visual motion cues has generally been attributed to the posteromedial lateral suprasylvian cortex (PMLS) (Toyama et al., 1985; Rauschecker et al., 1987; Rauschecker, 1988; Kim et al., 1997). The responses of neurons in this area are not critically dependent on inputs from the primary visual cortex (VC), as lesions of VC leave neuronal response properties in PMLS relatively unchanged (Spear & Baumann, 1979; Spear, 1988; Guido et al., 1990b). However, previous studies have used a limited range of visual stimuli. In this study, we assessed whether neurons in PMLS cortex remained direction-selective to complex motion stimuli following a lesion of VC, particularly to complex random dot kinematograms (RDKs). Unilateral aspiration of VC was performed on post-natal days 7–9. Single unit extracellular recordings were performed one year later in the ipsilateral PMLS cortex. As in previous studies, a reduction in the percentage of direction selective neurons was observed with drifting sinewave gratings. We report a previously unobserved phenomenon with sinewave gratings, in which there is a greater modulation of firing rate at the temporal frequency of the stimulus in animals with a lesion of VC, suggesting an increased segregation of ON and OFF sub-regions. A significant portion of neurons in PMLS cortex were direction selective to simple (16/18) and complex (11/16) RDKs. However, the strength of direction selectivity to both stimuli was reduced as compared to normals. The data suggest that complex motion processing is still present, albeit reduced, in PMLS cortex despite the removal of VC input. The complex RDK motion selectivity is consistent with both geniculo-cortical and extra-geniculate thalamo-cortical pathways in residual direction encoding.

scholarly journals Functional clusters of neurons in layer 6 of macaque V1

2019 ◽  
Author(s):  
Michael J Hawken ◽  
Robert M Shapley ◽  
Anita A Disney ◽  
Virginia Garcia-Marin ◽  
JA Henrie ◽  
...  
Keyword(s):  
Cluster Analysis ◽  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Temporal Frequency ◽  
Direction Selectivity ◽  
Frequency Bandwidth ◽  
Parallel Circuits ◽  
Response Measures ◽  
Visual Properties ◽  
Parameter Distributions

AbstracLayer 6 appears to perform a very important role in the function of macaque primary visual cortex, V1, but not enough is understood about the functional characteristics of neurons in the layer 6 population. It is unclear to what extent the population is homogeneous with respect to their visual properties or if one can identify distinct sub-populations. Here we performed a cluster analysis based on measurements of the responses of single neurons in layer 6 of primary visual cortex to achromatic grating stimuli that varied in orientation, direction of motion, spatial and temporal frequency, and contrast. The visual stimuli were presented in a stimulus window that was also varied in size. Using the responses to parametric variation in these stimulus variables we extracted a number of tuning response measures and used them in the cluster analysis. Six main clusters emerged along with some smaller clusters. Additionally we asked whether parameter distributions from each of the clusters were statistically different. There were clear separations of parameters between some of the clusters, particularly for f1/f0 ratio, direction selectivity, and temporal frequency bandwidth but other dimensions also showed differences between clusters. Our data suggest that in layer 6, across the spatial extent of a single cortical hypercolumn, there are multiple parallel circuits that provide information about different aspects of the visual stimulus.

scholarly journals Mechanisms of Direction Selectivity in Cat Primary Visual Cortex as Revealed by Visual Adaptation

2010 ◽  
Vol 104 (5) ◽  
pp. 2615-2623 ◽  
Author(s):  
Nicholas J. Priebe ◽  
Ilan Lampl ◽  
David Ferster
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Cortical Neurons ◽  
Visual Stimulation ◽  
Direction Selectivity ◽  
Dependent Manner ◽  
Visual Responses ◽  
Null Direction ◽  
Simple Cells ◽  
Complex Cells

In contrast to neurons of the lateral geniculate nucleus (LGN), neurons in the primary visual cortex (V1) are selective for the direction of visual motion. Cortical direction selectivity could emerge from the spatiotemporal configuration of inputs from thalamic cells, from intracortical inhibitory interactions, or from a combination of thalamic and intracortical interactions. To distinguish between these possibilities, we studied the effect of adaptation (prolonged visual stimulation) on the direction selectivity of intracellularly recorded cortical neurons. It is known that adaptation selectively reduces the responses of cortical neurons, while largely sparing the afferent LGN input. Adaptation can therefore be used as a tool to dissect the relative contribution of afferent and intracortical interactions to the generation of direction selectivity. In both simple and complex cells, adaptation caused a hyperpolarization of the resting membrane potential (−2.5 mV, simple cells, −0.95 mV complex cells). In simple cells, adaptation in either direction only slightly reduced the visually evoked depolarization; this reduction was similar for preferred and null directions. In complex cells, adaptation strongly reduced visual responses in a direction-dependent manner: the reduction was largest when the stimulus direction matched that of the adapting motion. As a result, adaptation caused changes in the direction selectivity of complex cells: direction selectivity was reduced after preferred direction adaptation and increased after null direction adaptation. Because adaptation in the null direction enhanced direction selectivity rather than reduced it, it seems unlikely that inhibition from the null direction is the primary mechanism for creating direction selectivity.

A model for the estimate of local image velocity by cells in the visual cortex

1990 ◽  
Vol 239 (1295) ◽  
pp. 129-161 ◽  
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Frequency Tuning ◽  
Temporal Frequency ◽  
Spatial Integration ◽  
Temporal Area ◽  
Image Velocity ◽  
Tuning Curves ◽  
Spatio Temporal ◽  
Local Image

Some computational theories of motion perception assume that the first stage en route to this perception is the local estimate of image velocity. However, this assumption is not supported by data from the primary visual cortex. Its motion sensitive cells are not selective to velocity, but rather are directionally selective and tuned to spatio-temporal frequen­cies. Accordingly, physiologically based theories start with filters selec­tive to oriented spatio-temporal frequencies. This paper shows that computational and physiological theories do not necessarily conflict, because such filters may, as a population, compute velocity locally. To prove this point, we show how to combine the outputs of a class of frequency tuned filters to detect local image velocity. Furthermore, we show that the combination of filters may simulate ‘Pattern’ cells in the middle temporal area (MT), whereas each filter simulates primary visual cortex cells. These simulations include three properties of the primary cortex. First, the spatio-temporal frequency tuning curves of the in­dividual filters display approximate space-time separability. Secondly, their direction-of-motion tuning curves depend on the distribution of orientations of the components of the Fourier decomposition and speed of the stimulus. Thirdly, the filters show facilitation and suppression for responses to apparent motions in the preferred and null directions, respect­ively. It is suggested that the MT’s role is not to solve the aperture problem, but to estimate velocities from primary cortex information. The spatial integration that accounts for motion coherence may be postponed to a later cortical stage.

scholarly journals Temporo-nasally biased moving grating selectivity in mouse primary visual cortex

2019 ◽  
Author(s):  
Marie Tolkiehn ◽  
Simon R. Schultz
Keyword(s):  
Visual Cortex ◽  
Spatial Frequency ◽  
Primary Visual Cortex ◽  
Moving Objects ◽  
Direction Selectivity ◽  
Orientation Tuning ◽  
High Signal ◽  
Forward Movement ◽  
Upward Moving

AbstractOrientation tuning in mouse primary visual cortex (V1) has long been reported to have a random or “salt-and-pepper” organisation, lacking the structure found in cats and primates. Laminar in-vivo multi-electrode array recordings here reveal previously elusive structure in the representation of visual patterns in the mouse visual cortex, with temporo-nasally drifting gratings eliciting consistently highest neuronal responses across cortical layers and columns, whilst upward moving gratings reliably evoked the lowest activities. We suggest this bias in direction selectivity to be behaviourally relevant as objects moving into the visual field from the side or behind may pose a predatory threat to the mouse whereas upward moving objects do not. We found furthermore that direction preference and selectivity was affected by stimulus spatial frequency, and that spatial and directional tuning curves showed high signal correlations decreasing with distance between recording sites. In addition, we show that despite this bias in direction selectivity, it is possible to decode stimulus identity and that spatiotemporal features achieve higher accuracy in the decoding task whereas spike count or population counts are sufficient to decode spatial frequencies implying different encoding strategies.Significance statementWe show that temporo-nasally drifting gratings (i.e. opposite the normal visual flow during forward movement) reliably elicit the highest neural activity in mouse primary visual cortex, whereas upward moving gratings reliably evoke the lowest responses. This encoding may be highly behaviourally relevant, as objects approaching from the periphery may pose a threat (e.g. predators), whereas upward moving objects do not. This is a result at odds with the belief that mouse primary visual cortex is randomly organised. Further to this biased representation, we show that direction tuning depends on the underlying spatial frequency and that tuning preference is spatially correlated both across layers and columns and decreases with cortical distance, providing evidence for structural organisation in mouse primary visual cortex.

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