Jérôme Ribot

Neurons in the primary visual cortex (V1) are classically thought to encode spatial features of visual stimuli through simple population codes: each neuron exhibits a preferred orientation and preferred spatial frequency, both of which remaining invariant to other aspects of the visual stimulus. Here, we show that this simple rule does not apply to the representation of major features of stimulus motion, including stimulus direction and temporal frequency (TF). We collected an extensive dataset of cat V1 responses to stimuli covarying in orientation, direction, spatial frequency, and TF to assess the extent of motion selectivity. We show that preferred TF is mostly uniform across the cortical surface. Yet, in over half of V1, the preferred direction is reversed with changing stimulus TF, revealing four distinct map motifs embedded in V1’s functional architecture. Similarly, despite the lack of spatial modulation for the preferred TF map and the lack of invariance for the preferred direction map, we found using convolutional neural networks that direction, TF and stimulus speed can be accurately decoded from V1 responses at all cortical locations. These findings suggest a latent encoding of information where subtle, spatially distributed modulations of V1 activity may convey fine information about stimulus motion, pointing to a novel primary sensory encoding mechanism despite complex co-variation of responses to multiple attributes across V1 neurons.

Perception of motion critically depends on detecting the speed and direction of moving stimuli. The primary visual cortex (V1) of some mammals, including primates and carnivores, exhibits functional organization for key receptive field properties such as orientation, direction, and spatial frequency; however, less is known about the organization of speed-tuned cells. While individual V1 neurons have been shown to exhibit speed selectivity, functional architecture for speed preference has been primarily reported in higher cortical areas such as primate area MT. Using multi-channel electrophysiology in anesthetized female ferrets, we investigated the joint tuning of V1 neurons for spatial frequency, temporal frequency, orientation/direction, and speed. We found significant clustering of cells tuned for speed and for speed preference within single electrode penetrations. We found that both simple and complex cells can exhibit speed tuning, and no strong variation across cortical layers. In reanalysis of intrinsic signal imaging data from cat V1, we observed repeating “hot spots” of high speed selectivity separated by “cold spots” with low tuning for speed. These findings indicate that a functional architecture for speed tuning is present within V1 itself and transmitted to downstream cortical regions. Significance Statement: To perceive moving objects, the visual system must detect both their direction and speed. The primary visual cortex, the first cerebral visual area to receive visual information from the retina via the lateral geniculate nucleus, plays a key role in this process. Here, we demonstrate that the primary visual cortex in carnivores contains speed-tuned neurons. Moreover, these neurons are organized into clustered “hot spots” that repeat across the cortical surface, suggesting a functional architecture for speed. While speed-tuned functional maps were previously thought to exist only in higher visual areas, such as area MT in primates, our findings reveal their presence at the level of primary visual cortex.

The ventrolateral preoptic nucleus (VLPO) of the hypothalamus plays a major role in the induction and consolidation of non-rapid eye movement (NREM) sleep. While VLPO neurons are heterogeneous, they often display low-threshold spikes (LTS), a feature that supports rhythmic activity. Nevertheless, rhythmic bursting in these VLPO neurons has never been observed. Here, we report that ∼12% of VLPO neurons in a large database of ex vivo patch-clamp recordings display spontaneous rhythmic bursting of action potentials. This activity occurred in putative sleep-promoting neurons, identified by inhibitory responses to noradrenaline (NA), as well as wake-active neurons that were activated by NA. Unsupervised clustering of 24 neurons based on burst properties, electrophysiological, and morphological features revealed three distinct groups: one corresponding to putative sleep-promoting neurons and two wake-active neurons with fast and slow bursting dynamics. Strikingly, membrane potential oscillations persisted in the presence of tetrodotoxin (TTX), indicating that rhythmic bursting is driven by intrinsic mechanisms rather than network activity. These findings suggest that rhythmic bursting is an intrinsic and functionally relevant mode of activity in VLPO neurons, which may contribute to sleep regulation.

Neurons in the primary visual cortex (V1) are classically thought to encode spatial features of visual stimuli through simple population codes: each neuron exhibits a preferred orientation and preferred spatial frequency, both of which remaining invariant to other aspects of the visual stimulus. Here, we show that this simple rule does not apply to the representation of major features of stimulus motion, including stimulus direction and temporal frequency (TF). We collected an extensive dataset of cat (of either sex) V1 responses to stimuli covarying in orientation, direction, spatial frequency, and TF to assess the extent of motion selectivity. We show that preferred TF is mostly uniform across the cortical surface. Yet, in over half of V1, the preferred direction is reversed with changing stimulus TF, revealing four distinct map motifs embedded in V1’s functional architecture. Similarly, despite the lack of spatial modulation for the preferred TF map and the lack of invariance for the preferred direction map, we found using convolutional neural networks that direction, TF and stimulus speed can be accurately decoded from V1 responses at all cortical locations. These findings suggest that subtle modulations of V1 activity may convey fine information about stimulus motion, pointing to a novel primary sensory encoding mechanism despite complex co-variation of responses to multiple attributes across V1 neurons. Significance Statement: Understanding how the external world is represented in the brain has long been a central endeavor in neuroscience. In the mammalian primary visual cortex (V1), groups of neurons encode stimulus properties through changes in activity, with “preferred” stimuli eliciting maximal responses, as demonstrated for orientation and spatial frequency. Using an extensive dataset of neuronal responses, we investigated whether V1 also encodes motion speed. We found that cortical response organization remains largely invariant, with neurons exhibiting a uniform preference for temporal frequency. Yet, machine learning algorithms decode motion speed with remarkable precision, revealing that subtle, spatially distributed modulations of activity underlie speed encoding. Moreover, we show that preferred direction flips with speed across 80% of cortex, uncovering a novel co-organization of motion and direction information in V1.

Médecine/sciences (M/S), revue internationale dans le domaine de la recherche biologique, médicale et en santé

How astrocytes close a critical period: During the visual critical period, brain circuits are rewired to adjust to sensory input. Closure of the critical period stabilizes the circuits. Looking at development in the mouse visual cortex, Ribot et al. found that astrocytes increase their expression of the gap junction channel subunit connexin 30, which in turn inhibits expression of a matrix-degrading enzyme (see the Perspective by Kofuji and Araque). As the matrix stabilizes, inhibitory interneurons mature, and the unusual flexibility of the critical period comes to an end. Science , abf5273, this issue p. 77 ; see also abj6745, p. 29

Summary paragraph: Brain postnatal development is characterized by critical periods of experience-dependent remodeling ^1,2 . Termination of these periods of intense plasticity is associated with settling of neuronal circuits, allowing for efficient information processing ³ . Failure to end critical periods thus results in neurodevelopmental disorders ^4,5 . Yet, the cellular processes defining the timing of these developmental periods remain unclear. Here we show in the mouse visual cortex that astrocytes control the closure of the critical period. We uncover a novel underlying pathway involving regulation of the extracellular matrix that allows interneurons maturation via an unconventional astroglial connexin signaling. We find that timing of the critical period closure is controlled by a marked developmental upregulation of the astroglial protein connexin 30 that inhibits expression of the matrix degrading enzyme MMP9 through the RhoA-GTPase signaling pathway. Our results thus demonstrate that astrocytes not only influence activity and plasticity of single synapses, but are also key elements in the experience-dependent wiring of brain developing circuits. This work, by revealing that astrocytes promote the maturation of inhibitory circuits, hence provide a new cellular target to alleviate malfunctions associated to impaired closure of critical periods.