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Construction of Perception from Touch Signals

Final Report Summary - CONCEPT (Construction of Perception from Touch Signals)

How does the brain transform the neuronal representation of a stimulus’s physical parameters into the neuronal representation of meaningful objects? An ideal platform for the inquiry is the rat whisker sensory system: it produces fast and accurate judgments of complex stimuli, yet can be broken down into accessible neuronal mechanisms. CONCEPT has examined the process that begins with whisker motion and ends with perception of the contacted object. There have been three main studies. In the first, we asked how the brain takes a decision on the basis of a stream of sensory input, one of the most pressing problems in cognitive neuroscience. A body of work has come to support a general framework whereby evidence is accumulated until the subject has acquired enough to make a choice. The bounded integration theory is elegant and has been worked out computationally. Its weakness is that nearly all support comes from a single paradigm: a monkey detecting the motion direction of a coherent set of dots within a random dot display. In CONCEPT we extended this core framework in three directions. First is the species: we test for bounded integration in rats rather than primates. Second is the sensory modality: we tested for bounded integration in the tactile rather than the visual modality. Third is the mode of operation of the sensorimotor network: we tested for bounded integration when the subject operates in the generative mode rather than the receptive mode. We found that rats move their whiskers along an object and generate sensory evidence according to the features of whisker shape and motion. These features constitute stimulus evidence, which is encoded by neurons in primary (vS1) and secondary (vS2) vibrissal somatosensory. The rat perceives the texture and makes a choice when the quantity of evidence accumulated by a downstream integrator reaches a boundary.

Evidence can be accumulated by active motion of the sensory receptors, as outlined above, or by acquiring a signal when the external object itself generates motion. In the second study, we developed a new behavioral task involving evidence accumulation and storage in working memory. Then, we examined neuronal activity in vS1, together with vibrissal motor cortex, vM1 (a frontal cortex target of vS1), while rats compared the intensity of two vibrations separated by an interstimulus delay. Vibrations were “noisy,” constructed by stringing together over time a sequence of velocity values sampled from a normal distribution. Psychometric curves reveal that rats overestimated the longer-duration stimulus—thus, perceived intensity of a vibration grew over the course of hundreds of milliseconds even while the sensory input remained, on average, stationary. Human subjects demonstrated the identical perceptual phenomenon, indicating that the underlying mechanisms of temporal integration generalize across species. The time dependence of the percept allowed us to ask to what extent neurons encoded the ongoing stimulus stream versus the animal’s percept. We demonstrated that vS1 firing correlated with the local features of the vibration, whereas vM1 firing correlated with the percept: the final vM1 population state varied, as did the rat’s behavior, according to both stimulus speed and stimulus duration. Moreover, vM1 populations appeared to participate in the trace of the percept of stimulus 1 as the rat awaited stimulus 2. In conclusion, the transformation of sensory data into the percept appears to involve the integration and storage of vS1 signals by vM1.

Knowledge about objects can be accessed through multiple sensory pathways. In the third study, we devised a task in which rats judged the orientation of a raised, black and white grating. Each trial required a visual (V), a tactile (T), or a visual-tactile (VT) discrimination; VT performance was better than that predicted by optimal linear combination of V and T signals, indicating synergy between sensory channels. Posterior parietal cortex (PPC) carried both graded information about object orientation and categorical information about the rat’s upcoming choice; single neurons exhibited identical responses under the three modality conditions. This study showed that PPC is involved in the supramodal processing of shape.

The three main studies, taken together, have helped us understand the general principles for the construction of perception, a step towards someday explaining why we experience the world as we do.