Nonuniform surround suppression of visual responses in mouse V1

Abstract

Complex receptive field characteristics, distributed across a population of neurons, are thought to be critical for solving perceptual inference problems that arise during motion and image segmentation. For example, in a class of neurons referred to as "end-stopped," increasing the length of stimuli outside of the bar-responsive region into the surround suppresses responsiveness. It is unknown whether these properties exist for receptive field surrounds in the mouse. We examined surround modulation in layer 2/3 neurons of the primary visual cortex in mice using two-photon calcium imaging. We found that surround suppression was significantly asymmetric in 17% of the visually responsive neurons examined. Furthermore, the magnitude of asymmetry was correlated with orientation selectivity. Our results demonstrate that neurons in mouse primary visual cortex are differentially sensitive to the addition of elements in the surround and that individual neurons can be described as being either uniformly suppressed by the surround, end-stopped, or side-stopped. NEW & NOTEWORTHY Perception of visual scenes requires active integration of both local and global features to successfully segment objects from the background. Although the underlying circuitry and development of perceptual inference is not well understood, converging evidence indicates that asymmetry and diversity in surround modulation are likely fundamental for these computations. We determined that these key features are present in the mouse. Our results support the mouse as a model to explore the neural basis and development of surround modulation as it relates to perceptual inference.

Keywords: mouse; orientation; primary visual cortex; receptive field; surround; vision.

Fig. 1.

Receptive field mapping. A: 2-photon GCaMP6f imaging within V1. PV-positive inhibitory neurons were labeled in red (yellow merge) and excluded from analysis. B: vertical and horizontal bars were used as stimuli to generate horizontal and vertical spatial tuning curves, respectively, for each neuron. Note that during surround modulation experiments, stimuli were randomly interleaved, and stimulus “off” responses were generally not observed and small when observed with smaller stimuli. C: examples of vertical and horizontal tuning curves based on the average of 3 trials (thin lines are single-trial responses). A contour of where the outer product of the tuning curves reaches less than 25% of its peak is shown to illustrate the 2-dimensional location of the receptive field with respect to the monitor. Twelve additional gray outlines of receptive fields are shown to illustrate the overlap within a single region from one session of two-photon imaging.

Fig. 2.

Surround modulation of receptive field responses for 3 individual neurons. A: 5 conditions were used to test the spatial properties of surround modulation. B–D: example average peak responses across trial (error bars are SE) when stimuli were shown only within the receptive field (black) and when stimuli were shown both within the receptive field and the surround (red and blue) for uniform surround (B), end-inhibition (C), and side-inhibition (D). *P < 0.05 indicates the criteria used to score a neuron as nonuniform; “ns” indicates not significant, thereby signifying that nonuniform facilitation was not detected.

Fig. 3.

Nonuniformity of surround modulation. For some neurons, the response to stimulus within the classical receptive field was significantly greater (P < 0.05) with bars in the collinear (lateral) surround regions vs. the lateral (collinear) surround regions (red and blue data points, respectively). Error bars are SE with respect to trials. Examples from Fig. 2 are noted by gold arrows.

Fig. 4.

Nonuniformity arises from lack of suppression in particular surround regions. A: neurons that respond significantly greater (P < 0.05) to classical receptive field stimuli with bars in the lateral surround are end-inhibited: they are strongly suppressed by collinear bars (red) with little or no suppression by lateral bars (blue). B: neurons that respond significantly greater (P < 0.05) to classical receptive field stimuli with bars in the collinear surround are side-inhibited: they are strongly suppressed by lateral bars (blue) with little or no suppression by collinear bars (red). Error bars are SE with respect to trials. Examples from Fig. 2 are noted by gold arrows.

Fig. 5.

Neurons with stronger nonuniformity in surround modulation have sharper orientation tuning. A: distribution of preferred orientations (there is a slight bias for horizontal orientations, 0°). Preferred orientation was calculated from the vector sum of the responses to the 4 orientations presented and binned into 6 groups. B: preferred orientations for all 24 significantly side- and end-inhibited neurons. Preferred orientation was calculated from the vector sum of the responses to the 4 orientations presented. NUI, nonuniformity index. C: orientation selectivity increases with greater nonuniformity in surround modulation for both lateral (n = 79, blue) and collinear (n = 59, red) condition-preferring neurons. D: population averages of orientation tuning divided into 3 groups on the basis of surround modulation nonuniformity. E: average orientation selectivity for the same 3 groups (error bars are SE based on neurons). ***P < 0.001.

Fig. 6.

Orientation selectivity does not depend or response magnitude. A: there is no significant correlation between orientation selectivity and response magnitude. B: there is no significant correlation between orientation selectivity and response noise. C: high-response data points for nonuniform surround neurons were dropped so that the average response magnitude for nonuniform surround neurons was less than or equal to the average response of uniform surround neurons. D: average orientation selectivity for the same 3 groups remained similar to that observed in Fig. 5 (error bars are SE based on neurons). **P < 0.01; ***P < 0.001.

Fig. 7.

Surround modulation nonuniformity is robust to changes in surround configuration. A: comparison of response magnitudes when the lateral surround is closer to (lateral close) or farther from (lateral far) the receptive field (inset). B: comparison of the nonuniformity index (NUI) between the lateral close and lateral far conditions. C: comparison of the distributions of NUIs for the lateral close and lateral far conditions. D: comparison of correlation between orientation selectivity and NUI between the lateral close and lateral far conditions.