Spatial integration during active tactile sensation drives elementary shape perception

Abstract

SummaryActive haptic sensation is critical for object identification and manipulation, such as for tool use in humans, or prey capture in rodents. The neural circuit basis for recognizing objects through active touch alone is poorly understood. To address this gap, we combined optogenetics, two photon imaging, and high-speed behavioral tracking in mice solving a novel surface orientation discrimination task with their whiskers. We found that orientation discrimination required animals to summate input from multiple whiskers specifically along the whisker arc. Many animals discriminated the orientation of the stimulus per se, as their performance was invariant to the specific location of the presented stimulus. Two photon imaging showed that populations of neurons in the barrel cortex encoded each of the discriminated orientations, and this coding depended on integration over the whisker array. Finally, acute optogenetic inactivation of the barrel cortex strongly impaired surface orientation discrimination, and even cell-type specific optogenetic suppression of layer 4 excitatory neurons degraded performance, implying a role for superficial layers in this computation. These data suggest a model in which spatial summation over an active haptic array generates representations of an object’s surface orientations. These computations may facilitate the encoding of complex three-dimensional objects during active exploration.

Behavioral and Neural Bases of Tactile Shape Discrimination Learning in Head-Fixed Mice

“…In mice, the means by which surface angles are determined with whiskers is unknown. It could require the integration of touch across multiple whiskers (Brown et al, 2020) via labeled line (Knutsen and Ahissar, 2009) or latency cues (Szwed et al, 2003). Alternatively, each whisker could function like a fingertip, providing sufficient information to perceive surface angles during active touch.…”

“…Neurons in the primary somatosensory cortex (S1) of anesthetized rodents encode direction-specific responses to passive whisker deflections (Andermann and Moore, 2006;Bruno et al, 2003;Kremer et al, 2011;Kwon et al, 2018;Lavzin et al, 2012;Simons and Carvell, 1989). S1 activity is required for active object orientation discrimination with multiple whiskers (Brown et al, 2020). Thus, S1 is a likely location of the neural representations of object angles and underlying sensory input.…”

The sensorimotor strategies and neuronal representations of tactile shape discrimination in mice

“…On the other hand, most tasks for head-fixed mice focus on spatially simple features, like the location of a pole or the texture of sandpaper (Chen et al, 2013; O 'Connor et al, 2010a). Indeed, the head-fixed mouse is often trimmed to a single whisker, though a few studies have considered multi-whisker behaviors (Brown et al, 2020;Celikel and Sakmann, 2007;Knutsen et al, 2006;Pluta et al, 2017).…”

Fast cortical dynamics encode tactile grating orientation during active touch

“…Therefore, the establishment of perceptual tasks such as the discrimination of grating orientation, three-dimensional bar orientation 25 To perform grating orientation discrimination in head-fixed conditions, mice need to execute a sequence of appropriate behaviors, much like humans do in object manipulation tasks 27 . The first action is to detect the incoming grating.…”