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The Journal of Neuroscience, October 29, 2008, 28(44):11205-11220; doi:10.1523/JNEUROSCI.2999-08.2008

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Behavioral/Systems/Cognitive
Vibrissa Sensation in Superior Colliculus: Wide-Field Sensitivity and State-Dependent Cortical Feedback

Jeremy D. Cohen, Akio Hirata, and Manuel A. Castro-Alamancos

Department of Neurobiology and Anatomy, Drexel University College of Medicine, Philadelphia, Pennsylvania 19129

Correspondence should be addressed to Dr. Manuel A. Castro-Alamancos, Department of Neurobiology and Anatomy, Drexel University College of Medicine, 2900 Queen Lane, Philadelphia, PA 19129. Email: mcastro{at}drexelmed.edu

Rodents use their vibrissae (whiskers) to sense and navigate the environment. A main target of this sensory information is the superior colliculus in the midbrain, which rats can use to detect meaningful whisker stimuli in behavioral contexts. Here, we used field potential, single-unit, and intracellular recordings to show that, although cells in the intermediate layers of the superior colliculus respond relatively effectively to single whiskers, the cells respond much more robustly to simultaneous, or nearly simultaneous, wide-field (multiwhisker) stimuli. The enhanced multiwhisker response is temporally stereotyped, consisting of two short latency peaks caused by convergent trigeminal synaptic inputs and cortical feedback, respectively. The cells are highly sensitive to the degree of temporal dispersion and contact order of multiwhisker stimuli, which makes them excellent detectors of initial multiwhisker contact. In addition, their output is most robust during quiescent states because of the dependence of cortical feedback on forebrain activation, and this may serve as an alerting signal to drive orienting responses.

Key words: superior colliculus; thalamus; barrel cortex; sensory processing; whisker; multiwhisker; rat; arousal

Received June 29, 2008; revised Aug. 29, 2008; accepted Sept. 7, 2008.

Correspondence should be addressed to Dr. Manuel A. Castro-Alamancos, Department of Neurobiology and Anatomy, Drexel University College of Medicine, 2900 Queen Lane, Philadelphia, PA 19129. Email: mcastro{at}drexelmed.edu






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