Behavioral Relevance of Fine Timing in Different Cortical Areas
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Neurons in sensory cortices can lock with millisecond precision to the fine timing of some stimuli, but it is not known whether or how this precision is used behaviorally. I addressed three issues related to these questions. First I asked whether fine timing differences in neural activity of auditory cortex are sufficient to drive behavior. Second I asked whether different cortical areas are differentially able to exploit timing information behaviorally. Finally I asked whether sensory deprivation affect the ability of resolving cortical timing.I used electrical microstimulation to establish a causal link between cortical timing information and behavior. I implanted two electrodes into the cortex of rats, and trained them to perform a two-alternative-forced-choice task in which the two stimuli to distinguish were simultaneous vs. sequential stimulation of the two electrodes. In this way I could bypass the sensory input and deliver stimuli directly to the cortex. I found that in auditory cortex, rats could exploit time differences as short as 3 msec to drive decisions, which suggests that precise neural timing in auditory cortex is sufficient to drive behavior. I also found that different cortical areas were different in deriving behaviorally relevant information from the fine timing of neural activity. In the visual cortex, animals could be trained to resolve differences of 15 msec but not 5 msec, substantially longer than the 3 msec limit observed in the auditory cortex. The barrel cortex was even"faster" than auditory cortex, with a lower limit below 1 msec. To determine whether this ability was use-dependent, I deprived rats of sensory input into the barrel cortex by trimming their whiskers from birth until adulthood, and trained them to distinguish fine timing differences in barrel cortex. All sensory deprived rats showed significant defects in discrimination, indicating that the ability to exploit cortical fine timing information is use-dependent. In conclusion, I found that: (1) precise cortical timing can drive behavior; (2) different sensory cortices have different thresholds; and (3) the ability to exploit timing information behaviorally is use-dependent. My findings have implications for the neural codes used by different sensory areas to encode information.