In Vivo Modulation of a Cortical
Functional Sensory Representation
Shortly After Topical Cholinergic
Agent Application
SILKE PENSCHUCK, CYNTHIA H. CHEN-BEE, NEAL PRAKASH, AND
RON D. FROSTIG
*
Department of Neurobiology and Behavior and the Center for the Neurobiology of
Learning and Memory, University of California at Irvine, Irvine, California 92697-4550
ABSTRACT
The aim of the present study was to determine whether cholinergic increase in the size
of a functional representation (collective evoked response from a large population of neurons)
can be observed shortly (within an hour) after treatment onset and whether nicotinic recep-
tors can participate in this type of modulation. Cholinergic agonist application has been found
previously to increase the response of a single cortical neuron to a stimulus. Also, pairing
cholinergic basal forebrain stimulation with delivery of a tone has been reported to increase
the size of that tone’s functional representation. Whereas the increase in a single cortical
neuron response can occur within seconds after cholinergic agonist application, to date the
increase in the size of a functional representation has only been investigated within one to
several weeks after the onset of pairing basal forebrain stimulation with tone delivery.
Furthermore, primarily muscarinic receptors have been implicated in these types of changes
in cortical activity. By using optical imaging of intrinsic signals in vivo, we found that the size
of a whisker’s functional representation in the primary somatosensory cortex of the rat
increases substantially within 69 or 46 minutes after topical application of either a musca-
rinic or nicotinic agonist to the exposed cortex, respectively, and decreases within 23 minutes
after topical application of a muscarinic antagonist. For each cholinergic agent, we verified
that delivery of a cholinergic agent by means of topical application can lead to the agent’s
successful penetration through the cortical layers in the time allotted to complete an imaging
experiment. Furthermore, the time course of penetration for each agent was characterized.
Based on the combined imaging/penetration results, we speculate on potential sites of cholinergic
action in the cortex. Irrespective of the exact mechanism of action, we demonstrate here that an
increase in the size of a functional sensory representation can occur shortly by means of activation of
either nicotinic or muscarinic receptors. J. Comp. Neurol. 452:38 –50, 2002. © 2002 Wiley-Liss, Inc.
Indexing terms: optical imaging; rat; primary somatosensory cortex; carbachol; nicotine;
scopolamine
The cholinergic basal forebrain (ACh-BF) has been im-
plicated in cortical processes such as attention, learning,
and memory (Richardson, 1991; Weinberger, 1993; Sarter
and Bruno, 1997). Currently, the cholinergic modulation
of these processes are only partially understood. Supply-
ing the main source of acetylcholine (ACh) to the cortex,
the cholinergic corticopetal projections originating from
the ACh-BF appear to play a role in modulating functional
sensory representations (cortical space occupied by neu-
rons responsive to a given sensory stimulus) in adult pri-
mary cortex (for review, see Weinberger, 1995; Dykes,
1997; Juliano, 1998; Edeline, 1999). For example, after
pairing a brief tone with a brief ACh-BF stimulation for
20 –25 days, the size of the paired tone’s functional repre-
Grant sponsor: NINDS; Grant number: NS-34519; Grant number: NS-
39760; Grant sponsor: NSF; Grant number: IBN-9507636; Grant sponsor:
Deutsche Forschungsgemeinschaft; Grant sponsor: Schweizer National Foun-
dation; Grant sponsor: Doehrenkamp-Zbinden Foundation; Grant sponsor:
American Heart Association Medical Student Research Fellowship
*Correspondence to: Ron D. Frostig, Department of Neurobiology and
Behavior, 2205 BioSci II, University of California at Irvine, Irvine, CA
92697-4550. E-mail: rfrostig@uci.edu
Received 12 February 2002; Revised 24 April 2002; Accepted 20 June 2002
DOI 10.1002/cne.10361
Published online the week of August 19, 2002 in Wiley InterScience
(www.interscience.wiley.com).
THE JOURNAL OF COMPARATIVE NEUROLOGY 452:38 –50 (2002)
© 2002 WILEY-LISS, INC.