A Cellular Resolution Map of Barrel Cortex Activity during Tactile Behavior.

Comprehensive measurement of neural activity remains challenging due to the large numbers of neurons in each brain area. We used volumetric two-photon imaging in mice expressing GCaMP6s and nuclear red fluorescent proteins to sample activity in 75% of superficial barrel cortex neurons across the relevant cortical columns, approximately 12,000 neurons per animal, during performance of a single whisker object localization task. Task-related activity peaked during object palpation. An encoding model related activity to behavioral variables. In the column corresponding to the spared whisker, 300 layer (L) 2/3 pyramidal neurons (17%) each encoded touch and whisker movements. Touch representation declined by half in surrounding columns; whisker movement representation was unchanged. Following the emergence of stereotyped task-related movement, sensory representations showed no measurable plasticity. Touch direction was topographically organized, with distinct organization for passive and active touch. Our work reveals sparse and spatially intermingled representations of multiple tactile features. VIDEO ABSTRACT.

Neural activity in barrel cortex underlying vibrissa-based object localization in mice.

Classical studies have related the spiking of selected neocortical neurons to behavior, but little is known about activity sampled from the entire neural population. We recorded from neurons selected independent of spiking, using cell-attached recordings and two-photon calcium imaging, in the barrel cortex of mice performing an object localization task. Spike rates varied across neurons, from silence to >60 Hz. Responses were diverse, with some neurons showing large increases in spike rate when whiskers contacted the object. Nearly half the neurons discriminated object location; a small fraction of neurons discriminated perfectly. More active neurons were more discriminative. Layer (L) 4 and L5 contained the highest fractions of discriminating neurons (∼63% and 79%, respectively), but a few L2/3 neurons were also highly discriminating. Approximately 13,000 spikes per activated barrel column were available to mice for decision making. Coding of object location in the barrel cortex is therefore highly redundant.

Precise subcellular input retinotopy and its computational consequences in an identified visual interneuron.

The Lobula Giant Movement Detector (LGMD) is a higher-order visual interneuron of Orthopteran insects that responds preferentially to objects approaching on a collision course. It receives excitatory input from an entire visual hemifield that anatomical evidence suggests is retinotopic. We show that this excitatory projection activates calcium-permeable nicotinic acetylcholine receptors. In vivo calcium imaging reveals that the excitatory projection preserves retinotopy down to the level of a single ommatidium. Examining the impact of retinotopy on the LGMD's computational properties, we show that sublinear synaptic summation can explain orientation preference in this cell. Exploring retinotopy's impact on directional selectivity leads us to infer that the excitatory input to the LGMD is intrinsically directionally selective. Our results show that precise retinotopy has implications for the dendritic integration of visual information in a single neuron.

Influence of electrotonic structure and synaptic mapping on the receptive field properties of a collision-detecting neuron.

The lobula giant movement detector (LGMD) is a visual interneuron of Orthopteran insects involved in collision avoidance and escape behavior. The LGMD possesses a large dendritic field thought to receive excitatory, retinotopic projections from the entire compound eye. We investigated whether the LGMD's receptive field for local motion stimuli can be explained by its electrotonic structure and the eye's anisotropic sampling of visual space. Five locust (Schistocerca americana) LGMD neurons were stained and reconstructed. We show that the excitatory dendritic field and eye can be fitted by ellipsoids having similar geometries. A passive compartmental model fit to electrophysiological data was used to demonstrate that the LGMD is not electrotonically compact. We derived a spike rate to membrane potential transform using intracellular recordings under visual stimulation, allowing direct comparison between experimental and simulated receptive field properties. By assuming a retinotopic mapping giving equal weight to each ommatidium and equally spaced synapses, the model reproduced the experimental data along the eye equator, though it failed to reproduce the receptive field along the ventral-dorsal axis. Our results illustrate how interactions between the distribution of synaptic inputs and the electrotonic properties of neurons contribute to shaping their receptive fields.