Cerebral Cortex, Vol 8, 346-361, Copyright © 1998 by Oxford University Press
N Almassy, GM Edelman and O Sporns
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 translation-invariant 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.
ARTICLES
Behavioral constraints in the development of neuronal properties: a cortical model embedded in a real-world device
The Neurosciences Institute, San Diego, CA 92121, USA.
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