Abstract
In principle, the development of sensory receptive fields in cortex could arise from experience-independent mechanisms that have been acquired through evolution, or through an online analysis of the sensory experience of the individual animal. Here we review recent experiments that suggest that the development of direction selectivity in carnivore visual cortex requires experience, but also suggest that the experience of an individual animal cannot greatly influence the parameters of the direction tuning that emerges, including direction angle preference and speed tuning. The direction angle preference that a neuron will acquire can be predicted from small initial biases that are present in the naïve cortex prior to the onset of visual experience. Further, experience with stimuli that move at slow or fast speeds does not alter the speed tuning properties of direction-selective neurons, suggesting that speed tuning preferences are built in. Finally, unpatterned optogenetic activation of the cortex over a period of a few hours is sufficient to produce the rapid emergence of direction selectivity in the naïve ferret cortex, suggesting that information about the direction angle preference that cells will acquire must already be present in the cortical circuit prior to experience. These results are consistent with the idea that experience has a permissive influence on the development of direction selectivity.
Highlights
Orientation selectivity is present at the onset of visual experience but direction selectivity requires visual experience At the time of eye opening, neurons in primary visual cortex of cats and ferrets already exhibit substantial selectivity for stimulus orientation [16–20]
We present evidence a b from a series of recent studies from our group that suggests that while experience is necessary for the development of direction selectivity, the parameters of the direction tuning that develops are largely determined before the onset of visual experience
We have argued that the bulk of the present evidence suggests that experience has a permissive role in the development of direction selectivity in ferret visual cortex
Summary
It is apparent that many features of our behavior, and features of our brains, are learned. One could have reasonably argued whether the entire visual system, including cells selective for high-level features like faces, could really be built from scratch, but modern deep learning systems that are trained on enormous sets of data, such as a huge repository of images and videos on the internet, exhibit the ability to identify objects or faces (e.g., [8, 9]). Deep learning unit response properties resemble those of early visual cortical neurons, while higher layers can exhibit selectivity for classes of objects or faces, much like neurons in the inferior temporal (IT) cortex in primates [10–12] This argument shows that a “thought analysis” of the information processing problem to be solved by the visual system (Marr’s “first level”) [13], in this case, does not usefully constrain broad ideas about nature vs nurture with respect to how primary sensory neurons develop in mammals. We argue that visual experience has a largely permissive role in the development of direction selectivity
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