Thalamocortical inputs trigger a propagating envelope of gamma-band activity in auditory cortex in vitro.
To investigate how auditory cortex responds to thalamic inputs, we have used electrophysiological and anatomical techniques to characterize a brain slice containing functionally linked thalamocortical and intracortical pathways. In extracellular recordings, stimulation of thalamic afferents elicited a short-latency field potential and current sink in layer IV of the cortex, followed by 100-500 ms of polysynaptic activity containing rapid (gamma-band, 20-80 Hz) fluctuations. Paired intracellular and extracellular recordings showed that a short-latency excitatory postsynaptic potential (EPSP) corresponded to the fast extracellular potential, and that a slow intracellular depolarization with superimposed rapid fluctuations corresponded to the polysynaptic extracellular activity. Pharmacological manipulations demonstrated that glutamate receptors contributed to mono- and polysynaptic activity, and that the gamma-band fluctuations contained intermixed rapid depolarizations and Cl(-)-mediated inhibition. The spread of evoked activity through auditory cortex was determined by extracellular mapping away from the excitatory focus (the site of the largest amplitude fast response). The short-latency potential traversed auditory cortex at 1.25 m/s and decreased over 1-2 mm, likely reflecting sequential activation of cells contacted by thalamocortical arbors. In contrast, polysynaptic activity did not decrease but propagated as a spatially restricted wave at a 57-fold slower velocity (0.022 m/s). Thus, stimulation of the auditory thalamocortical pathway in vitro elicited a fast glutamatergic potential in layer IV, followed by polysynaptic activity, including gamma-band fluctuations, that propagated through the cortex. Propagating activity may form transient neural assemblies that contribute to auditory information processing.
Metherate
R
R
Department of Psychobiology, University of California, Irvine, 92697-4550, USA. rmethera@uci.edu
Cruikshank
S J
SJ
D015763:2-Amino-5-phosphonovalerate / Q000494:pharmacology; D018750:6-Cyano-7-nitroquinoxaline-2,3-dione / Q000494:pharmacology; D000818:Animals; D001303:Auditory Cortex / Q000033:anatomy & histology / Q000502:physiology*; D001306:Auditory Pathways / Q000033:anatomy & histology / Q000502:physiology*; D001931:Brain Mapping; D002540:Cerebral Cortex / Q000033:anatomy & histology / Q000502:physiology*; D004558:Electric Stimulation; D018691:Excitatory Amino Acid Antagonists / Q000494:pharmacology; D019706:Excitatory Postsynaptic Potentials / Q000187:drug effects / Q000502:physiology; D051379:Mice; D008815:Mice, Inbred Strains; D010852:Picrotoxin / Q000494:pharmacology; D011189:Potassium Chloride / Q000494:pharmacology; D051381:Rats; D017207:Rats, Sprague-Dawley; D011930:Reaction Time; D013569:Synapses / Q000187:drug effects / Q000502:physiology; D009435:Synaptic Transmission / Q000187:drug effects / Q000502:physiology; D013788:Thalamus / Q000033:anatomy & histology / Q000502:physiology*
D015763:2-Amino-5-phosphonovalerate; D018750:6-Cyano-7-nitroquinoxaline-2,3-dione; D018691:Excitatory Amino Acid Antagonists; D010852:Picrotoxin; D011189:Potassium Chloride