SummaryCortical computation arises from the interaction of multiple neuronal types, including pyramidal (Pyr) cells and interneurons expressing Sst, Vip, or Pvalb. To study the circuit underlying such interactions, we imaged these four types of cells in mouse primary visual cortex (V1). Our recordings in darkness were consistent with a “disinhibitory” model in which locomotion activates Vip cells, thus inhibiting Sst cells and disinhibiting Pyr cells. However, the disinhibitory model failed when visual stimuli were present: locomotion increased Sst cell responses to large stimuli and Vip cell responses to small stimuli. A recurrent network model successfully predicted each cell type’s activity from the measured activity of other types. Capturing the effects of locomotion, however, required allowing it to increase feedforward synaptic weights and modulate recurrent weights. This network model summarizes interneuron interactions and suggests that locomotion may alter cortical computation by changing effective synaptic connectivity.
SummaryPrimary visual cortex exhibits two types of gamma rhythm: broadband activity in the 30–90 Hz range and a narrowband oscillation seen in mice at frequencies close to 60 Hz. We investigated the sources of the narrowband gamma oscillation, the factors modulating its strength, and its relationship to broadband gamma activity. Narrowband and broadband gamma power were uncorrelated. Increasing visual contrast had opposite effects on the two rhythms: it increased broadband activity, but suppressed the narrowband oscillation. The narrowband oscillation was strongest in layer 4 and was mediated primarily by excitatory currents entrained by the synchronous, rhythmic firing of neurons in the lateral geniculate nucleus (LGN). The power and peak frequency of the narrowband gamma oscillation increased with light intensity. Silencing the cortex optogenetically did not abolish the narrowband oscillation in either LGN firing or cortical excitatory currents, suggesting that this oscillation reflects unidirectional flow of signals from thalamus to cortex.
Summary At various stages of the visual system, visual responses are modulated by arousal. Here, we find that in mice this modulation operates as early as in the first synapse from the retina and even in retinal axons. To measure retinal activity in the awake, intact brain, we imaged the synaptic boutons of retinal axons in the superior colliculus. Their activity depended not only on vision but also on running speed and pupil size, regardless of retinal illumination. Arousal typically reduced their visual responses and selectivity for direction and orientation. Recordings from retinal axons in the optic tract revealed that arousal modulates the firing of some retinal ganglion cells. Arousal had similar effects postsynaptically in colliculus neurons, independent of activity in the other main source of visual inputs to the colliculus, the primary visual cortex. These results indicate that arousal modulates activity at every stage of the mouse visual system.
In the mouse primary visual cortex (V1), sensory responses are shaped by behavioral factors such as locomotion. These factors are thought to control a disinhibitory circuit, whereby interneurons expressing vasoactive intestinal peptide (Vip) inhibit those expressing somatostatin (Sst), disinhibiting pyramidal cells (Pyr). We measured the effect of locomotion on these neurons and on interneurons expressing parvalbumin (Pvalb) in layer 2/3 of mouse V1, and found inconsistencies with the disinhibitory model. In the presence of large stimuli, locomotion increased Sst cell responses without suppressing Vip cells. In the presence of small stimuli, locomotion increased Vip cell responses without suppressing Sst cells. A circuit model could reproduce each cell type's activity from the measured activity of other cell types, but only if we allowed locomotion to increase feedforward synaptic weights while modulating recurrent weights. These results suggest that locomotion alters cortical function by changing effective synaptic connectivity, rather than only through disinhibition.
Posterior parietal cortex (PPC) has been implicated in navigation, in the control of movement, and in visually-guided decisions. To relate these views, we measured activity in PPC while mice performed a virtual navigation task driven by visual decisions. PPC neurons were selective for specific combinations of the animal's spatial position and heading angle. This selectivity closely predicted both the activity of individual PPC neurons, and the arrangement of their collective firing patterns in choice-selective sequences. These sequences reflected PPC encoding of the animal’s navigation trajectory. Using decision as a predictor instead of heading yielded worse fits, and using it in addition to heading only slightly improved the fits. Alternative models based on visual or motor variables were inferior. We conclude that when mice use vision to choose their trajectories, a large fraction of parietal cortex activity can be predicted from simple attributes such as spatial position and heading.
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