Orientation-Tuned Surround Suppression in Mouse Visual Cortex

Abstract

The firing rates of neurons in primary visual cortex (V1) are suppressed by large stimuli, an effect known as surround suppression. In cats and monkeys, the strength of suppression is sensitive to orientation; responses to regions containing uniform orientations are more suppressed than those containing orientation contrast. This effect is thought to be important for scene segmentation, but the underlying neural mechanisms are poorly understood. We asked whether it is possible to study these mechanisms in the visual cortex of mice, because of recent advances in technology for studying the cortical circuitry in mice. It is unknown whether neurons in mouse V1 are sensitive to orientation contrast. We measured the orientation selectivity of surround suppression in the different layers of mouse V1. We found strong surround suppression in layer 4 and the superficial layers, part of which was orientation tuned: iso-oriented surrounds caused more suppression than cross-oriented surrounds. Surround suppression was delayed relative to the visual response and orientation-tuned suppression was delayed further, suggesting two separate suppressive mechanisms. Previous studies proposed that surround suppression depends on the activity of inhibitory somatostatin-positive interneurons in the superficial layers. To test the involvement of the superficial layers we topically applied lidocaine. Silencing of the superficial layers did not prevent orientation-tuned suppression in layer 4. These results show that neurons in mouse V1, which lacks orientation columns, show orientation-dependent surround suppression in layer 4 and the superficial layers and that surround suppression in layer 4 does not require contributions from neurons in the superficial layers.

Single 5 μm diameter needle electrode block modules for unit recordings in vivo

“…Although conventional metal electrodes are often used to isolate cells in layer 2/3, the smaller microelectrodes used in this study are potentially better suited to isolating activity of single cells in the cortex. Neurons within layer 2/3 are currently being studied because they correspond to highly ordered information processing in high-density neuronal circuits192021.…”

Circuits and Mechanisms for Surround Modulation in Visual Cortex

“…Strongest suppression is induced by stimuli in the RF and surround of the same orientation, spatial frequency, drift direction, and speed, and weaker suppression or facilitation is induced by stimuli of orthogonal parameters (e.g., orthogonally oriented stimuli or stimuli drifting in opposite directions) (DeAngelis et al 1994, Li & Li 1994, Sengpiel et al 1997, Walker et al 1999, Cavanaugh et al 2002a, Müller et al 2003, Webb et al 2005, Henry et al 2013, Self et al 2014). Importantly, the orientation tuning of SM is independent of the orientation preference of the recorded neurons: strongest suppression occurs for iso-oriented stimuli in the RF and surround, even if the stimulus in the RF is not at the neuron’s preferred orientation (Sillito et al 1995, Cavanaugh et al 2002b, Shushruth et al 2012), provided that such a stimulus evokes a response from the neuron when presented in the RF alone (Shushruth et al 2012).…”

“…This is because in mouse, a large fraction of LGN cells have orientation- and direction-selective RFs (Marshel et al 2012, Piscopo et al 2013, Scholl et al 2013, Zhao et al 2013), and orientation-tuned surround suppression emerges in layer 4 as fast as in other V1 layers and does not require intact superficial layers (Self et al 2014). …”

A Disinhibitory Circuit for Contextual Modulation in Primary Visual Cortex

“…In a different context, obtained by changing the orientation of the gratings in the surround, surround suppression in excitatory neurons is weakened and their responses may even be facilitated (Self et al, 2014;Slllito et al, 1995;Walker et al, 1999). Yet, the mechanisms that eliminate surround suppression remain elusive.…”