Understanding circuit properties from physiological data presents two challenges: (i) recordings do not reveal connectivity, and (ii) stimuli only exercise circuits to a limited extent. We address these challenges for the mouse visual system with a novel neural manifold obtained using unsupervised algorithms. Each point in our manifold is a neuron; nearby neurons respond similarly in time to similar parts of a stimulus ensemble. This ensemble includes drifting gratings and flows, i.e., patterns resembling what a mouse would “see” running through fields. Regarding (i), our manifold differs from the standard practice in computational neuroscience: embedding trials in neural coordinates. Topology matters: we infer that, if the circuit consists of separate components, the manifold is discontinuous (illustrated with retinal data). If there is significant overlap between circuits, the manifold is nearly-continuous (cortical data). Regarding (ii), most of the cortical manifold is not activated with conventional gratings, despite their prominence in laboratory settings. Our manifold suggests organizing cortical circuitry by a few specialized circuits for specific members of the stimulus ensemble, together with circuits involving ‘multi-stimuli’-responding neurons. To approach real circuits, local neighborhoods in the manifold are identified with actual circuit components. For retinal data, we show these components correspond to distinct ganglion cell types by their mosaic-like receptive field organization, while for cortical data, neighborhoods organize neurons by type (excitatory/inhibitory) and anatomical layer. In summary: the topology of neural organization reflects well the underlying anatomy and physiology of the retina and the visual cortex.
more »
« less
Encoding manifolds constructed from grating responses organize responses to natural scenes in cortical visual areas
We have created encoding manifolds to reveal the overall responses of a brain area to a variety of stimuli. Encoding manifolds organize response properties globally: each point on an encoding manifold is a neuron, and nearby neurons respond similarly to the stimulus ensemble in time. We previously found, using a large stimulus ensemble including optic flows, that encoding manifolds for the retina were highly clustered, with each cluster corresponding to a different ganglion cell type. In contrast, the topology of the V1 manifold was continuous. Now, using responses of individual neurons from the Allen Institute Visual Coding-Neuropixels dataset in the mouse, we infer encoding manifolds for V1 and for five higher cortical visual areas (VISam, VISal, VISpm, VISlm, and VISrl). We show here that the encoding manifold topology computed only from responses to various grating stimuli is also continuous, not only for V1 but also for the higher visual areas, with smooth coordinates spanning it that include, among others, orientation selectivity and firing-rate magnitude. Surprisingly, the encoding manifold for gratings also provides information about natural scene responses. To investigate whether neurons respond more strongly to gratings or natural scenes, we plot the log ratio of natural scene responses to grating responses (mean firing rates) on the encoding manifold. This reveals a global coordinate axis organizing neurons' preferences between these two stimuli. This coordinate is orthogonal (i.e., uncorrelated) to that organizing firing rate magnitudes in VISp. Analyzing layer responses, a preference for gratings is concentrated in layer 6, whereas preference for natural scenes tends to be higher in layers 2/3 and 4. We also find that preference for natural scenes dominates the responses of neurons that prefer low (0.02 cpd) and high (0.32 cpd) spatial frequencies, rather than intermediate ones (0.04 to 0.16 cpd). Conclusion: while gratings seem limited and natural scenes unconstrained, machine learning algorithms can reveal subtle relationships between them beyond linear techniques.
more »
« less
- Award ID(s):
- 1822598
- PAR ID:
- 10553354
- Publisher / Repository:
- bioRxiv.org
- Date Published:
- Format(s):
- Medium: X
- Institution:
- bioRxiv
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Assessments of the mouse visual system based on spatial-frequency analysis imply that its visual capacity is low, with few neurons responding to spatial frequencies greater than 0.5 cycles per degree. However, visually mediated behaviors, such as prey capture, suggest that the mouse visual system is more precise. We introduce a stimulus class—visual flow patterns—that is more like what the mouse would encounter in the natural world than are sine-wave gratings but is more tractable for analysis than are natural images. We used 128-site silicon microelectrodes to measure the simultaneous responses of single neurons in the primary visual cortex (V1) of alert mice. While holding temporal-frequency content fixed, we explored a class of drifting patterns of black or white dots that have energy only at higher spatial frequencies. These flow stimuli evoke strong visually mediated responses well beyond those predicted by spatial-frequency analysis. Flow responses predominate in higher spatial-frequency ranges (0.15–1.6 cycles per degree), many are orientation or direction selective, and flow responses of many neurons depend strongly on sign of contrast. Many cells exhibit distributed responses across our stimulus ensemble. Together, these results challenge conventional linear approaches to visual processing and expand our understanding of the mouse’s visual capacity to behaviorally relevant ranges.more » « less
-
Abstract To produce consistent sensory perception, neurons must maintain stable representations of sensory input. However, neurons in many regions exhibit progressive drift across days. Longitudinal studies have found stable responses to artificial stimuli across sessions in visual areas, but it is unclear whether this stability extends to naturalistic stimuli. We performed chronic 2-photon imaging of mouse V1 populations to directly compare the representational stability of artificial versus naturalistic visual stimuli over weeks. Responses to gratings were highly stable across sessions. However, neural responses to naturalistic movies exhibited progressive representational drift across sessions. Differential drift was present across cortical layers, in inhibitory interneurons, and could not be explained by differential response strength or higher order stimulus statistics. However, representational drift was accompanied by similar differential changes in local population correlation structure. These results suggest representational stability in V1 is stimulus-dependent and may relate to differences in preexisting circuit architecture of co-tuned neurons.more » « less
-
The retina and primary visual cortex (V1) both exhibit diverse neural populations sensitive to diverse visual features. Yet it remains unclear how neural populations in each area partition stimulus space to span these features. One possibility is that neural populations are organized into discrete groups of neurons, with each group signaling a particular constellation of features. Alternatively, neurons could be continuously distributed across feature-encoding space. To distinguish these possibilities, we presented a battery of visual stimuli to the mouse retina and V1 while measuring neural responses with multi-electrode arrays. Using machine learning approaches, we developed a manifold embedding technique that captures how neural populations partition feature space and how visual responses correlate with physiological and anatomical properties of individual neurons. We show that retinal populations discretely encode features, while V1 populations provide a more continuous representation. Applying the same analysis approach to convolutional neural networks that model visual processing, we demonstrate that they partition features much more similarly to the retina, indicating they are more like big retinas than little brains.more » « less
-
The tilt illusion—a bias in the perceived orientation of a center stimulus induced by an oriented surround—illustrates how context shapes visual perception. Although extensively studied for decades, we still lack a comprehensive account of the illusion that connects its behavioral and neural characteristics. Here, we demonstrate that the tilt illusion originates from dynamic changes in neural coding precision induced by the surround context. We simultaneously obtained psychophysical and functional MRI responses from human subjects while they viewed gratings in the absence and presence of an oriented surround and independently extracted sensory encoding precision from their behavioral and neural data. Both measures show that in the absence of an oriented surround, encoding reflects the natural scene statistics of orientation. However, with an oriented surround, encoding precision is significantly increased for stimuli similar to the surround orientation. This local change in encoding is sufficient to predict the behavioral characteristics of the tilt illusion using a Bayesian observer model. The effect of surround modulation increases along the ventral stream and is localized to the portion of the visual cortex with receptive fields at the center-surround boundary. The pattern of change in coding accuracy reflects the surround-conditioned orientation statistics in natural scenes, but cannot be explained by local stimulus configuration. Our results suggest that the tilt illusion naturally emerges from an adaptive coding strategy that efficiently reallocates neural coding resources based on the current stimulus context.more » « less
An official website of the United States government

