scholarly journals Distinct spatiotemporal mechanisms underlie extra-classical receptive field modulation in macaque V1 microcircuits

2019 ◽  
Author(s):  
Christopher A. Henry ◽  
Mehrdad Jazayeri ◽  
Robert M. Shapley ◽  
Michael J. Hawken

AbstractComplex scene perception depends upon the interaction between signals from the classical receptive field (CRF) and the extra-classical receptive field (eCRF) in primary visual cortex (V1) neurons. While much is known about V1 eCRF properties, it remains unknown how the underlying mechanisms map onto the cortical microcircuit. We probed the spatio-temporal dynamics of eCRF modulation using a reverse correlation paradigm, and found three principal eCRF mechanisms: tuned-facilitation, untuned-suppression, and tuned-suppression. Each mechanism had a distinct timing and spatial profile. Laminar analysis showed that the timing, orientation-tuning, and strength of eCRF mechanisms had distinct signatures within magnocellular and parvocellular processing streams in the V1 microcircuit. The existence of multiple eCRF mechanisms provides new insights into how V1 responds to spatial context. Modeling revealed that the differences in timing and scale of these mechanisms predicted distinct patterns of net modulation, reconciling many previous disparate physiological and psychophysical findings.

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Christopher A Henry ◽  
Mehrdad Jazayeri ◽  
Robert M Shapley ◽  
Michael J Hawken

Complex scene perception depends upon the interaction between signals from the classical receptive field (CRF) and the extra-classical receptive field (eCRF) in primary visual cortex (V1) neurons. Although much is known about V1 eCRF properties, we do not yet know how the underlying mechanisms map onto the cortical microcircuit. We probed the spatio-temporal dynamics of eCRF modulation using a reverse correlation paradigm, and found three principal eCRF mechanisms: tuned-facilitation, untuned-suppression, and tuned-suppression. Each mechanism had a distinct timing and spatial profile. Laminar analysis showed that the timing, orientation-tuning, and strength of eCRF mechanisms had distinct signatures within magnocellular and parvocellular processing streams in the V1 microcircuit. The existence of multiple eCRF mechanisms provides new insights into how V1 responds to spatial context. Modeling revealed that the differences in timing and scale of these mechanisms predicted distinct patterns of net modulation, reconciling many previous disparate physiological and psychophysical findings.


1998 ◽  
Vol 80 (6) ◽  
pp. 2882-2892 ◽  
Author(s):  
Christopher I. Moore ◽  
Sacha B. Nelson

Moore, Christopher I. and Sacha B. Nelson. Spatio-temporal subthreshold receptive fields in the vibrissa representation of rat primary somatosensory cortex. J. Neurophysiol. 80: 2882–2892, 1998. Whole cell recordings of synaptic responses evoked by deflection of individual vibrissa were obtained from neurons within adult rat primary somatosensory cortex. To define the spatial and temporal properties of subthreshold receptive fields, the spread, amplitude, latency to onset, rise time to half peak amplitude, and the balance of excitation and inhibition of subthreshold input were quantified. The convergence of information onto single neurons was found to be extensive: inputs were consistently evoked by vibrissa one- and two-away from the vibrissa that evoked the largest response (the “primary vibrissa”). Latency to onset, rise time, and the incidence and strength of inhibitory postsynaptic potentials (IPSPs) varied as a function of position within the receptive field and the strength of evoked excitatory input. Nonprimary vibrissae evoked smaller amplitude subthreshold responses [primary vibrissa, 9.1 ± 0.84 (SE) mV, n = 14; 1-away, 5.1 ± 0.5 mV, n = 38; 2-away, 3.7 ± 0.59 mV, n = 22; 3-away, 1.3 ± 0.70 mV, n = 8] with longer latencies (primary vibrissa, 10.8 ± 0.80 ms; 1-away, 15.0 ± 1.2 ms; 2-away, 15.7 ± 2.0 ms). Rise times were significantly faster for inputs that could evoke action potential responses (suprathreshold, 4.1 ± 1.3 ms, n = 8; subthreshold, 12.4 ± 1.5 ms, n = 61). In a subset of cells, sensory evoked IPSPs were examined by deflecting vibrissa during injection of hyperpolarizing and depolarizing current. The strongest IPSPs were evoked by the primary vibrissa ( n = 5/5), but smaller IPSPs also were evoked by nonprimary vibrissae ( n = 8/13). Inhibition peaked by 10–20 ms after the onset of the fastest excitatory input to the cortex. This pattern of inhibitory activity led to a functional reversal of the center of the receptive field and to suppression of later-arriving and slower-rising nonprimary inputs. Together, these data demonstrate that subthreshold receptive fields are on average large, and the spatio-temporal dynamics of these receptive fields vary as a function of position within the receptive field and strength of excitatory input. These findings constrain models of suprathreshold receptive field generation, multivibrissa interactions, and cortical plasticity.


2001 ◽  
Vol 86 (5) ◽  
pp. 2559-2570 ◽  
Author(s):  
Masaharu Kinoshita ◽  
Hidehiko Komatsu

The perceived brightness of a surface is determined not only by the luminance of the surface (local information), but also by the luminance of its surround (global information). To better understand the neural representation of surface brightness, we investigated the effects of local and global luminance on the activity of neurons in the primary visual cortex (V1) of awake macaque monkeys. Single- and multiple-unit recordings were made from V1 while the monkeys were performing a visual fixation task. The classical receptive field of each neuron was identified as a region responding to a spot stimulus. Neural responses were assessed using homogeneous surfaces at least three times as large as the receptive field as stimuli. We first examined the sensitivity of neurons to variation in local surface luminance, while the luminance of the surround was held constant. The activity of a large majority of surface-responsive neurons (106/115) varied monotonically with changes in surface luminance; in some the dynamic range was over 3 log units. This monotonic relation between surface luminance and neural activity was more evident later in the stimulus period than early on. The effect of the global luminance on neural activity was then assessed in 81 of the surface-responsive neurons by varying the luminance of the surround while holding the luminance of the surface constant. The activity of one group of neurons (25/81) was unaffected by the luminance of the surround; these neurons appear to encode the physical luminance of a surface covering the receptive field. The responses of the other neurons were affected by the luminance of the surround. The effects of the luminances of the surface and the surround on the activities of 26 of these neurons were in the same direction (either increased or decreased), while the effects on the remaining 25 neurons were in opposite directions. The activities of the latter group of neurons seemed to parallel the perceived brightness of the surface, whereas the former seemed to encode the level of illumination. There were differences across different types of neurons with regard to the layer distribution. These findings indicate that global luminance information significantly modulates the activity of surface-responsive V1 neurons and that not only physical luminance, but also perceived brightness, of a homogeneous surface is represented in V1.


2003 ◽  
Vol 20 (3) ◽  
pp. 221-230 ◽  
Author(s):  
BEN S. WEBB ◽  
CHRIS J. TINSLEY ◽  
NICK E. BARRACLOUGH ◽  
AMANDA PARKER ◽  
ANDREW M. DERRINGTON

Gain control is a salient feature of information processing throughout the visual system. Heeger (1991, 1992) described a mechanism that could underpin gain control in primary visual cortex (V1). According to this model, a neuron's response is normalized by dividing its output by the sum of a population of neurons, which are selective for orientations covering a broad range. Gain control in this scheme is manifested as a change in the semisaturation constant (contrast gain) of a V1 neuron. Here we examine how flanking and annular gratings of the same or orthogonal orientation to that preferred by a neuron presented beyond the receptive field modulate gain in V1 neurons in anesthetized marmosets (Callithrix jacchus). To characterize how gain was modulated by surround stimuli, the Michaelis–Menten equation was fitted to response versus contrast functions obtained under each stimulus condition. The modulation of gain by surround stimuli was modelled best as a divisive reduction in response gain. Response gain varied with the orientation of surround stimuli, but was reduced most when the orientation of a large annular grating beyond the classical receptive field matched the preferred orientation of neurons. The strength of surround suppression did not vary significantly with retinal eccentricity or laminar distribution. In the marmoset, as in macaques (Angelucci et al., 2002a, b), gain control over the sort of distances reported here (up to 10 deg) may be mediated by feedback from extrastriate areas.


2010 ◽  
Vol 1 (3) ◽  
pp. 35-35 ◽  
Author(s):  
M. A. Smith ◽  
W. Bair ◽  
J. R. Cavanaugh ◽  
J. A. Movshon

2018 ◽  
Vol 120 (2) ◽  
pp. 409-420 ◽  
Author(s):  
Corey M. Ziemba ◽  
Jeremy Freeman ◽  
Eero P. Simoncelli ◽  
J. Anthony Movshon

The stimulus selectivity of neurons in V1 is well known, as is the finding that their responses can be affected by visual input to areas outside of the classical receptive field. Less well understood are the ways selectivity is modified as signals propagate to visual areas beyond V1, such as V2. We recently proposed a role for V2 neurons in representing the higher order statistical dependencies found in images of naturally occurring visual texture. V2 neurons, but not V1 neurons, respond more vigorously to “naturalistic” images that contain these dependencies than to “noise” images that lack them. In this work, we examine the dependency of these effects on stimulus size. For most V2 neurons, the preference for naturalistic over noise stimuli was modest when presented in small patches and gradually strengthened with increasing size, suggesting that the mechanisms responsible for this enhanced sensitivity operate over regions of the visual field that are larger than the classical receptive field. Indeed, we found that surround suppression was stronger for noise than for naturalistic stimuli and that the preference for large naturalistic stimuli developed over a delayed time course consistent with lateral or feedback connections. These findings are compatible with a spatially broad facilitatory mechanism that is absent in V1 and suggest that a distinct role for the receptive field surround emerges in V2 along with sensitivity for more complex image structure. NEW & NOTEWORTHY The responses of neurons in visual cortex are often affected by visual input delivered to regions of the visual field outside of the conventionally defined receptive field, but the significance of such contextual modulations are not well understood outside of area V1. We studied the importance of regions beyond the receptive field in establishing a novel form of selectivity for the statistical dependencies contained in natural visual textures that first emerges in area V2.


2014 ◽  
Vol 96 ◽  
pp. 87-95 ◽  
Author(s):  
Ke Chen ◽  
Xue-Mei Song ◽  
Zheng-Qiang Dai ◽  
Jiao-Jiao Yin ◽  
Xing-Zhen Xu ◽  
...  

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