Early sensory pathways for detection of fearful conditioned stimuli: tectal and thalamic relays

Jeremy David Cohen

doi:10.17918/00000630

This work set out to elucidate early sensory pathways underlying detection of conditioned stimuli that mediate performance of a fear-motivated active avoidance behavior. The well-defined rat trigeminal somatosensory system was used as a model in these studies to assess which sensory afferent pathways are critical for successful performance of the learned behavior. Vibrissal-based somatosensory information enters the central nervous system via the trigeminal ganglion and reaches the brainstem trigeminal complex. From there, two major ascending sensory pathways extend toward the forebrain and midbrain tectum. One reaches the contralateral somatosensory thalamus and is termed the trigeminothalamic pathway. Another pathway reaches the contralateral superior colliculus and is termed the trigeminotectal pathway. From the thalamus, tactile information is relayed to the primary somatosensory cortex (S1), which is known to send a feedback projection to the ipsilateral superior colliculus. In chapter 2, we employed reversible and irreversible lesions of the somatosensory thalamus and/or superior colliculus prior to performance on the active avoidance task and show that the tectal and thalamic relays can function independently to mediate the signal detection required for successful performance. In addition, we show that the critical nature of the sensory pathways is dependent on the fear conditioning paradigm, as lesions of the somatosensory thalamus, but flot superior colliculus, disrupt expression of a Pavlovian fear conditioned behavior. The surprising ability of the superior colliculus to detect meaningful whisker information prompted us to characterize whisker-evoked responses in superior colliculus cells. In chapter 3, we show that while cells of the superior colliculus respond relatively effectively to stimulation of single whiskers, the cells respond much more robustly to simultaneous, or nearly simultaneous, wide-field (multiwhisker) stimuli. The response to multiwhisker stimulation consists of two short-latency peaks (peak1 and peak2). Peak1 is a sharp rising response caused by the convergence of trigeminotectal cells primarily representing the activity of a single whisker. In contrast, peak2 is a slower rising and broader response that is largely caused by descending inputs from somatosensory cortex. Interestingly, we report that peak2 is suppressed during forebrain activation. This suggests that the output of the superior colliculus, and thus, the impact on downstream target structures, is most robust for multiwhisker stimuli during behaviorally quiescent states. The functional independence of the trigeminothalamic and trigeminotectal pathways (chapter 2) and the particular sensitivity of trigeminotectal responses for more salient wide-field stimuli (chapter 3) led us to conduct additional behavioral studies testing the effects of pathway inactivation on detection of low salience stimuli. In chapter 4, we show that detection of a low salience stimulus requires that both the tectal and thalamic relays be available, suggesting a functional synergy of these sensory pathways. This finding prompted us to compare the impact of low and high salience stimuli on barrel cortex and superior colliculus responses in alert animals. We show that low salience stimuli produce significantly smaller responses in both regions than those produced by high salience stimuli, which suggests a distributed and sparse coding for low salience stimuli. Together, this work serves to outline a somatosensory signal detection circuitry that is highly dynamic and functionally dependent on the behavioral state of the animal.

Early sensory pathways for detection of fearful conditioned stimuli: tectal and thalamic relays

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Early sensory pathways for detection of fearful conditioned stimuli: tectal and thalamic relays

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