Journal of Neurochemist,y
Lippincott—Raven Publishers, Philadelphia
© 1998 International Society for Neurochemistry
Histamine H
1 Receptor Antagonists Produce Increases
in Extracellular Acetyicholine in Rat Frontal Cortex
and Hippocampus
Hans C. Dringenberg, M. Angelica De Souza-Silva, Jens Roßmüller,
Joseph P. Huston, and Rainer K. W. Schwarting
Institute of Physiological Psychology I and Center for Biological and Medical Research, Heinrich-Heine University
Düsseldorf Düsseldoif Germany
Abstract: Lesions of the neuronal histaminergic system
or pharmacological blockade of histamine receptors, e.g.,
with histamine H1 receptor antagonists, can enhance the
performance of rats in several tests of learning and mem-
ory. The underlying neuronal systems that mediate these
behavioral effects are not known. Here, we examined the
effects of treatment with histamine H1 antagonists on ex-
tracellular levels of acetylcholine (ACh) in adult rats anes-
thetized with urethane (1.25 g/kg). ACh was quantified
using in vivo microdialysis and HPLC with electrochemi-
cal detection. Basal levels of ACh in the frontal cortex
and hippocampus were in the range of 0.54 ±0.13 and
0.96 ± 0.17 pmol/20 mm, respectively. Injection (intraper-
itoneally) of saline did not produce significant increases
in ACh levels, even though there was a slight and gradual
increase in cortical ACh levels throughout the course of
the experiments (up to 4h after an injection). Administra-
tion of the H1 receptor antagonist chlorpheniramine (intra-
peritoneally) produced a dose-dependent increase of cor-
tical ACh levels to a maximum of 260, 280, and 570%
of baseline values after doses of 5, 10, and 20 mg/kg,
respectively. In the hippocampus, ACh content increased
to a maximum of —.600% of baseline levels after chlor-
pheniramine administration (20 mg/kg, i.p.). Administra-
tion of the H1 antagonist pyrilamine (intraperitoneally) in-
creased cortical ACh content to a maximum of 300 and
500%, whereas hippocampal ACh levels increased to 215
and 280% after doses of 10 and 20 mg/kg, respectively.
In an additional experiment using nonanesthetized, freely
moving rats, cortical ACh content showed a moderate
increase (to 190%) after saline injections (intraperitone-
ally) and a much higher increase (to 370%) after chlorphe-
niramine treatment (20 mg/kg, i.p.). These data suggest
that cortical and hippocampal levels of ACh can be effec-
tively modulated by systemic treatment with histamine H1
antagonists. The increases in ACh levels produced by H1
antagonists may suggest that some histaminergic recep-
tors exert an inhibitory influence over central ACh levels.
The enhanced availability of ACh in the forebrain may
contribute to the behavioral effects observed with H1 an-
tagonist treatment. Key Words: Acetylcholine—Histamine
—H1 antagonists—Neocortex—Hippocampus—
Microdialysis.
J. Neurochem. 70, 1750—1758 (1998).
The cholinergic innervation of the cortical mantle
arises predominantly from cholinergic cell groups in
the basal forebrain that include the substantia innomi-
nata, ventral pallidum, globus pallidus, nucleus basalis
magnocellularis, and horizontal limb of the diagonal
band of Broca, whereas the medial septum and vertical
diagonal band of Broca provide the cholinergic in-
nervation of the hippocampal formation (Divac, 1975;
Big! et a!., 1982; Mesulam et a!., 1983; Saper, 1984;
Luiten et a!., 1987; Semba and Fibiger, 1989; Woolf,
1991). Numerous hypotheses exist with regard to the
behavioral functions controlled by these cholinergic
projection systems. In rats and monkeys, cholinergic
deficits related to lesions, pharmacological blockade,
or aging can produce severe impairments in both spe-
cies-specific behaviors, e.g., general activity, sexual
behavior, and food hoarding, and in tests of learning
and memory, such as avoidance or discrimination
learning, or spatial navigation (Singer, 1968; Dubois
et al., 1985; Whishaw et al., 1985; Collerton, 1986;
Stroessner-Johnson et al., 1992; Quirion et al., 1995;
Dornan et al., 1996). Thus, it appears that intact cholin-
ergic transmission contributes importantly to various
behavioral capacities, even though the underlying pro-
cesses, e.g., ‘‘attention,‘‘ ‘‘storage,‘‘ and ‘‘retrieval,‘‘
involved remain controversial (Fibiger, 1991; Blok-
land, 1996; Thiel et al., 1998).
The importance of cholinergic transmission in be-
havioral performance is widely recognized, but the role
of complex interactions between cholinergic and other
transmitter systems is less well understood. Several
transmitter-specific cell populations (serotonergic, nor-
Received July 11, 1997; revised manuscript received October 28,
1997; accepted November 24, 1997.
Address correspondence and reprint requests to Dr. R. K. W.
Schwarting at Institute of Physiological Psychology I, Heinrich-
Heine University Düsseldorf, Universitätsstrasse 1, 40225 Düssel-
dorf, Germany.
Abbreviations used: ACh, acetylcholine; TM, tuberomammillary
nucleus.
1750