scholarly journals Anatomy and Physiology of Macaque Visual Cortical Areas V1, V2, and V5/MT: Bases for Biologically Realistic Models

2020 ◽  
Vol 30 (6) ◽  
pp. 3483-3517 ◽  
Author(s):  
Simo Vanni ◽  
Henri Hokkanen ◽  
Francesca Werner ◽  
Alessandra Angelucci

Abstract The cerebral cortex of primates encompasses multiple anatomically and physiologically distinct areas processing visual information. Areas V1, V2, and V5/MT are conserved across mammals and are central for visual behavior. To facilitate the generation of biologically accurate computational models of primate early visual processing, here we provide an overview of over 350 published studies of these three areas in the genus Macaca, whose visual system provides the closest model for human vision. The literature reports 14 anatomical connection types from the lateral geniculate nucleus of the thalamus to V1 having distinct layers of origin or termination, and 194 connection types between V1, V2, and V5, forming multiple parallel and interacting visual processing streams. Moreover, within V1, there are reports of 286 and 120 types of intrinsic excitatory and inhibitory connections, respectively. Physiologically, tuning of neuronal responses to 11 types of visual stimulus parameters has been consistently reported. Overall, the optimal spatial frequency (SF) of constituent neurons decreases with cortical hierarchy. Moreover, V5 neurons are distinct from neurons in other areas for their higher direction selectivity, higher contrast sensitivity, higher temporal frequency tuning, and wider SF bandwidth. We also discuss currently unavailable data that could be useful for biologically accurate models.

2010 ◽  
Vol 5 (1) ◽  
pp. 21-30 ◽  
Author(s):  
Alice Rokszin ◽  
Zita Márkus ◽  
Gábor Braunitzer ◽  
Antal Berényi ◽  
Marek Wypych ◽  
...  

AbstractOur study compares the spatio-temporal visual receptive field properties of different subcortical stages of the ascending tectofugal visual system. Extracellular single-cell recordings were performed in the superficial (SCs) and intermediate (SCi) layers of the superior colliculus (SC), the suprageniculate nucleus (Sg) of the posterior thalamus and the caudate nucleus (CN) of halothane-anesthetized cats. Neuronal responses to drifting gratings of various spatial and temporal frequencies were recorded. The neurons of each structure responded optimally to low spatial and high temporal frequencies and displayed narrow spatial and temporal frequency tuning. The detailed statistical analysis revealed that according to its stimulus preferences the SCs has markedly different spatio-temporal properties from the homogeneous group formed by the SCi, Sg and CN. The SCs neurons preferred higher spatial and lower temporal frequencies and had broader spatial tuning than the other structures. In contrast to the SCs the visually active SCi, as well as the Sg and the CN neurons possessed consequently similar spatio-temporal preferences. These data support our hypothesis that the visually active SCi, Sg and CN neurons form a homogeneous neuronal population given a similar spatio-temporal frequency preference and a common function in processing of dynamic visual information.


1999 ◽  
Vol 11 (3) ◽  
pp. 300-311 ◽  
Author(s):  
Edmund T. Rolls ◽  
Martin J. Tovée ◽  
Stefano Panzeri

Backward masking can potentially provide evidence of the time needed for visual processing, a fundamental constraint that must be incorporated into computational models of vision. Although backward masking has been extensively used psychophysically, there is little direct evidence for the effects of visual masking on neuronal responses. To investigate the effects of a backward masking paradigm on the responses of neurons in the temporal visual cortex, we have shown that the response of the neurons is interrupted by the mask. Under conditions when humans can just identify the stimulus, with stimulus onset asynchronies (SOA) of 20 msec, neurons in macaques respond to their best stimulus for approximately 30 msec. We now quantify the information that is available from the responses of single neurons under backward masking conditions when two to six faces were shown. We show that the information available is greatly decreased as the mask is brought closer to the stimulus. The decrease is more marked than the decrease in firing rate because it is the selective part of the firing that is especially attenuated by the mask, not the spontaneous firing, and also because the neuronal response is more variable at short SOAs. However, even at the shortest SOA of 20 msec, the information available is on average 0.1 bits. This compares to 0.3 bits with only the 16-msec target stimulus shown and a typical value for such neurons of 0.4 to 0.5 bits with a 500-msec stimulus. The results thus show that considerable information is available from neuronal responses even under backward masking conditions that allow the neurons to have their main response in 30 msec. This provides evidence for how rapid the processing of visual information is in a cortical area and provides a fundamental constraint for understanding how cortical information processing operates.


1989 ◽  
Vol 2 (6) ◽  
pp. 609-620 ◽  
Author(s):  
A. B. Saul ◽  
M. S. Cynader

AbstractAdaptation-induced changes in the temporal-frequency tuning and direction selectivity of cat visual cortical cells were studied. Aftereffects were induced largely independent of direction. Adapting in either direction reduced responses in both directions. Aftereffects in the direction opposite that adapted were only slightly weaker than were aftereffects in the adapted direction. No cell showed any enhancement of responses to drifting test stimuli after adapting with moving gratings. Adapting in a cell's null direction usually had no effect. Dramatic differences between the adaptation characteristics of moving and stationary stimuli were observed, however.Furthermore, aftereffects were temporal frequency specific. Temporal frequency-specific aftereffects were found in both directions: adapting in one direction induced frequency-specific effects in both directions. This bidirectionality of frequency-specific aftereffects applied to the spatial domain as well. Often, aftereffects in the direction opposite that adapted were more narrowly tuned.In general, adaptation could shift a cell's preferred temporal frequency. Aftereffects were most prominent at high temporal frequencies when testing in the adapted direction. Aftereffects seemed to be more closely linked to temporal frequency than to velocity matching.These results constrain models of cortical connectivity. In particular, we argue against schemes by which direction selectivity is generated by inhibiting a cell specifically when stimulated in the nonpreferred direction. Instead, we argue that cells receive bidirectional spatially and temporally tuned inputs, which could combine in spatiotemporal quadrature to produce direction selectivity.


2015 ◽  
Vol 113 (7) ◽  
pp. 2605-2617 ◽  
Author(s):  
Henry J. Alitto ◽  
W. Martin Usrey

Extraclassical surround suppression strongly modulates responses of neurons in the retina, lateral geniculate nucleus (LGN), and primary visual cortex. Although a great deal is known about the spatial properties of extraclassical suppression and the role it serves in stimulus size tuning, relatively little is known about how extraclassical suppression shapes visual processing in the temporal domain. We recorded the spiking activity of retinal ganglion cells and LGN neurons in the cat to test the hypothesis that extraclassical suppression influences temporal features of visual responses in the early visual system. Our results demonstrate that extraclassical suppression not only shifts the distribution of interspike intervals in a manner that decreases the efficacy of neuronal communication, it also decreases the reliability of neuronal responses to visual stimuli and it decreases the duration of visual responses, an effect that underlies a rightward shift in the temporal frequency tuning of LGN neurons. Taken together, these results reveal a dynamic relationship between extraclassical suppression and the temporal features of neuronal responses.


2005 ◽  
Vol 94 (2) ◽  
pp. 1336-1345 ◽  
Author(s):  
Bartlett D. Moore ◽  
Henry J. Alitto ◽  
W. Martin Usrey

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.


1998 ◽  
Vol 80 (6) ◽  
pp. 2991-3004 ◽  
Author(s):  
Allen L. Humphrey ◽  
Alan B. Saul

Humphrey, Allen L. and Alan B. Saul. 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.


1992 ◽  
Vol 8 (4) ◽  
pp. 365-372 ◽  
Author(s):  
Alan B. Saul ◽  
Allen L. Humphrey

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.


2016 ◽  
Vol 145 (6) ◽  
pp. 672-707 ◽  
Author(s):  
Simona Buetti ◽  
Deborah A. Cronin ◽  
Anna M. Madison ◽  
Zhiyuan Wang ◽  
Alejandro Lleras

2001 ◽  
Vol 38-40 ◽  
pp. 1379-1383 ◽  
Author(s):  
A.E. Krukowski ◽  
T.W. Troyer ◽  
K.D. Miller

2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Eugenio Piasini ◽  
Liviu Soltuzu ◽  
Paolo Muratore ◽  
Riccardo Caramellino ◽  
Kasper Vinken ◽  
...  

AbstractCortical representations of brief, static stimuli become more invariant to identity-preserving transformations along the ventral stream. Likewise, increased invariance along the visual hierarchy should imply greater temporal persistence of temporally structured dynamic stimuli, possibly complemented by temporal broadening of neuronal receptive fields. However, such stimuli could engage adaptive and predictive processes, whose impact on neural coding dynamics is unknown. By probing the rat analog of the ventral stream with movies, we uncovered a hierarchy of temporal scales, with deeper areas encoding visual information more persistently. Furthermore, the impact of intrinsic dynamics on the stability of stimulus representations grew gradually along the hierarchy. A database of recordings from mouse showed similar trends, additionally revealing dependencies on the behavioral state. Overall, these findings show that visual representations become progressively more stable along rodent visual processing hierarchies, with an important contribution provided by intrinsic processing.


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