The ability of organisms to categorize diverse and often novel stimuli depends on ongoing interactions with their environment. In a modality such as vision, categorization requires the generation of both selective and invariant responses of cortical neurons to complex visual stimuli. How does behavior contribute to shaping the responses of these neurons? Analysis of this question is made difficult by the complex multilevel interactions between many neural and behavioral variables. To mitigate this difficulty, we studied the development and ongoing plasticity of pattern-selective neuronal responses by means of synthetic neural modeling. For this purpose, we constructed Darwin V, which consists of a simulated neuronal model embedded in a real-world device that is capable of motion and autonomous behavior. The neuronal model consists of four major components: a visual system (containing cortical and subcortical networks); a taste system based on conductance; sets of motor neurons capable of triggering behavior; and a diffuse ascending (value) system. The modeled visual cortex consists of two areas: a topographic map responsive to elementary features connected to a higher-order map composed of initially non-selective neuronal units. During behavior over time in its environment, Darwin V encounters numerous objects consisting of black metal cubes displaying different patterns of white blobs and stripes. Initially, the lack of specific higher-order visual responses does not allow visual pattern discrimination, and appetitive and aversive behaviors are triggered by the 'taste' (surface conductivity of objects) alone. In the course of sensory experience, however, changes occur in visual and sensorimotor connection strengths, with two major consequences. First, units within the higher visual area acquire responses that are both pattern selective and translation invariant. Second, as a result of the operation of the value system, these responses become linked to appropriate behaviors. Analysis of Darwin V after such changes indicates that the continuity of self-generated movements is essential for the development of pattern-selective and translationinvariant responses. The concomitant development of a preference for foveal over parafoveal objects was found to be due to increased behavioral interactions with object cubes gripped by the centrally mounted effector (snout) of Darwin V. Finally, even after development of higher-order visual responses, visual responses to more frequently encountered objects continued to be enhanced, while other responses were diminished. Overall, the detailed study of Darwin V over multiple levels of organization provides a heuristically revealing example of the crucial role played by behavioral and environmental interactions in the development of complex responses by specialized neurons.
Adaptive behavior requires the sensing of salient behavioral consequences which can act to modulate changes in neural connections linking sensory and motor structures. In previous work, we proposed that salient sensory events trigger neuronal value systems capable of modulating synaptic plasticity. Here, we investigate the capacity of value systems to modulate their own responses in the context of various conditioning tasks. To this end, we implement a modifiable value system incorporating anatomical and physiological properties within Darwin V, a neuronal model embedded in a mobile real world device. While exploring an environment containing stimulus objects, Darwin V's visual maps develop object-related neuronal responses. Phasic responses of a value system initially triggered only by object-"taste" (innate value) modulate changes in connections between visual and motor neurons, thus linking specific visual responses to appropriate motor outputs. Over time, Darwin V is able behaviorally to discriminate between "striped" objects with positive value (appetitive behavior) and objects with "blobs" with negative value (aversive behavior) based on vision alone. In parallel with modification of visuo-motor connections, value-dependent modification also occurs in connections from visual sensory maps to the value system itself. As a result, visual activity patterns become able directly to trigger value signals (acquired value). If acquired value is disabled, transfer of the value signal to stimuli preceding innately salient events does not occur, and behavioral responses due to aversive conditioning are subject to rapid extinction. If an auditory signal reliably precedes the visual appearance of an aversive object, Darwin V could be conditioned first to reject the object based on vision (primary conditioning), and subsequently based on sound alone (secondary conditioning). We compare the functional characteristics of value-dependent learning to formal notions of reinforcement learning. We suggest that plasticity in sensory afferents to value systems may provide a neurobiological basis for mediating the changing effects of saliency on adaptive behavioral responses.
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