Morphological heterogeneity within the cingulate cortex in rat: a horseradish peroxidase transport study

doi:10.1016/0006-8993(91)91661-J

Brain Research

Volume 565, Issue 2, 29 November 1991, Pages 290-300

https://doi.org/10.1016/0006-8993(91)91661-J Get rights and content

Abstract

We compared the connections of two areas within rat cingulate cortex, the Cg1/Cg2 area vs the Cg3 area, by iontophoresing small quantities of wheatgerm agglutinin-horseradish peroxidase (WGA-HRP) into either of these two divisions and identifying afferent and efferent connections. Cortical projections were more widespread for the cingulate cortex (Cg3) area than for the Cg1/Cg2 area and included the dysgranular and agranular insular cortex, and perirhinal cortex. The Cg3 area received input from the CA1 layer of the hippocampus while the Cg1/Cg2 area was interconnected primarily with retrosplenial cortex. In the brainstem, both received input from Barrington's nucleus, however, many of the subcortical connections of the two areas differed and supported the hypothesis that the Cg3 area is part of the limbic and visceral motor system while the Cg1/Cg2 area is more closely allied with somatic motor control. The Cg3 area received input from the basolateral nucleus of the amygdala, the supramammillary hypothalamic nucleus, the laterodorsal tegmental nucleus, and the lateral parabrachial nucleus. The Cg1/Cg2 area received input from the substantia nigra and targeted deep layers of the superior colliculus Thus, rat cingulate cortex is a heterogeneous area that can be further subdivided into separate limbic/autonomic (Cg3) and somatic motor areas (Cg1/Cg2).

References (50)

J.C. Adams
Stabilizing and rapid thionin staining of TMB-based HRP reaction product
Neurosci. Lett.
(1980)
S. Burns et al.
The involvement of the anterior cingulate cortex in blood pressure control
Brain Research
(1985)
R.D. Hall et al.
Organization of motor and somatosensory neocortex in the albino rat
Brain Research
(1974)
J.W. Hubbard et al.
Parabrachial lesions increase plasma norepinephrine concentration, plasma renin activity and enhance baroreflex sensitivity in the conscious rat
Brain Research
(1987)
K.M. Hurley-Gius et al.
The medial frontal cortex and gastric motility: microstimulation results and their possible significance for the overall pattern of organization of rat frontal and parietal cortex
Brain Research
(1986)
T.M. Jay et al.
Selectivity of the hippocampal projection to the prelimbic area of the prefrontal cortex in the rat
Brain Research
(1989)
R.P. Kesner et al.
Dissociation of item and order spatial memory in rat following medial prefrontal cortex lesions
Neuropsychology
(1987)
R.P. Kesner
Memory for frequency in rats: role of the hippocampus and medial prefrontal cortex
Behav. Neurol. Biol.
(1990)
C.M. Leonard
The prefrontal cortex of the rat. I. Cortical projection of the mediodorsal nucleus. II. Efferent connections
Brain Research
(1969)
A.D. Loewy et al.
Descending projections from the pontine micturition center
Brain Research
(1979)

E.J. Neafsey et al.

The organization of the rat motor cortex: a microstimulation mapping study

Brain Res. Rev.

(1986)

K. Satoh et al.

Localization of the micturition reflex center at the dorsolateral pontine tegmentum of the rat

Neurosci. Lett.

(1978)

W.A. Suzuki et al.

Cortical inputs to the CA1 field of the monkey hippocampus originate from the perirhinal and parahippocampal cortex but not from area TE

Neurosci. Lett.

(1990)

L.W. Swanson

A direct projection from Ammon's horn to prefrontal cortex in the rat

Brain Research

(1981)

R.R. Terreberry et al.

Rat medial frontal cortex: a visceral motor region with a direct projection to the solitary nucleus

Brain Research

(1983)

R.R. Terreberry et al.

The rat medial frontal cortex projects directly to autonomic regions of the brainstem

Brain Res. Bull.

(1987)

D. Van Der Kooy et al.

Visceral cortex: a direct connection from prefrontal cortex to the solitary nucleus in rat

Neurosci. Lett.

(1982)

A.J. Verberne et al.

Medial prefrontal cortical lesions modulate baroreflex sensitivity in the rat

Brain Research

(1987)

D.G. Ward

Stimulation of the parabrachial with monosodium glutamate increases arterial pressure

Brain Research

(1988)

T. Yamamoto et al.

Aversive taste stimuli increase CGRP levels in the gustatory insular cortex of the rat

Neurosci. Lett.

(1990)

H. Al Maskati et al.

Stimulation in prefrontal cortex area inhibits cardiovascular and motor components of the defence reaction in rats

J. Auton. Nerv. Syst.

(1989)

R.M. Beckstead

Convergent thalamic and mesencephalic projections to the anterior medial cortex in the rat

J. Comp. Neurol.

(1976)

R.M. Beckstead

An autoradiographic examination of corticocortical and subcortical projections of the mediodorsal-projection (prefrontal) cortex of the rat

J. Comp. Neurol.

(1979)

J.F. Donoghue et al.

The motor cortex of the rat: cytoarchitecture and microstimulation mapping

J. Comp. Neurol.

(1982)

F. Ferino et al.

Anatomical and electrophysiological evidence for a direct projection from Ammon's horn to the medial prefrontal cortex in the rat

Exp. Brain Res.

(1987)

Cited by (25)

Limbic circuitry activation in ethanol withdrawal is regulated by a chromosome 1 locus
2017, Alcohol
Citation Excerpt :
This work expands upon our previous work comparing the two progenitor strains, with D2 strain mice showing significantly greater withdrawal-associated c-Fos induction than the B6 strain in the PrL and BLA following chronic alcohol exposure (Chen et al., 2009), and the Cg1 and dorsolateral STR using an acute withdrawal model (Kozell et al., 2005). The PrL has direct projections to the amygdala including the BLA (Mcdonald, Mascagni, & Guo, 1996) and other limbic structures (Deniau, Menetrey, & Charpier, 1996; Gabbott, Warner, Jays, Salway, & Busby, 2005), whereas the Cg1 projects to the dorsal STR and other structures (Gabbott et al., 2005; Mitrofanis & Mikuletic, 1999; Sesack, Deutch, Roth, & Bunney, 1989), and receives inputs from the BLA and SNr (Zeng & Stuesse, 1991). Taken together, our results point to the involvement of an extended limbic circuit in mediating Alcdp1/Alcw1 actions, providing mechanistic (brain regional) information.
Physiological dependence and associated withdrawal episodes are thought to constitute a motivational force sustaining alcohol use/abuse and contributing to relapse in alcoholics. Although no animal model exactly duplicates alcoholism, models for specific factors, including the withdrawal syndrome, are useful for identifying potential genetic and neural determinants of liability in humans. We previously identified highly significant quantitative trait loci (QTLs) with large effects on predisposition to withdrawal after chronic and acute alcohol exposure in mice and mapped these loci to the same region of chromosome 1 (Alcdp1 and Alcw1, respectively). The present studies utilize a novel Alcdp1/Alcw1 congenic model (in which an interval spanning Alcdp1 and Alcw1 from the C57BL/6J donor strain [build GRCm38 150.3–174.6 Mb] has been introgressed onto a uniform inbred DBA/2J genetic background) known to demonstrate significantly less severe chronic and acute withdrawal compared to appropriate background strain animals. Here, using c-Fos induction as a high-resolution marker of neuronal activation, we report that male Alcdp1/Alcw1 congenic animals demonstrate significantly less alcohol withdrawal-associated neural activation compared to appropriate background strain animals in the prelimbic and cingulate cortices of the prefrontal cortex as well as discrete regions of the extended amygdala (i.e., basolateral) and extended basal ganglia (i.e., dorsolateral striatum, and caudal substantia nigra pars reticulata). These studies are the first to begin to elucidate circuitry by which this confirmed addiction-relevant QTL could influence behavior. This circuitry overlaps limbic circuitry involved in stress, providing additional mechanistic information. Alcdp1/Alcw1 maps to a region syntenic with human chromosome 1q, where multiple studies find significant associations with risk for alcoholism.
Circuit-Based Corticostriatal Homologies Between Rat and Primate
2016, Biological Psychiatry
Understanding the neural mechanisms of psychiatric disorders requires the use of rodent models; however, frontal-striatal homologies between rodents and primates are unclear. In contrast, within the striatum, the shell of the nucleus accumbens, the hippocampal projection zone, and the amygdala projection zone (referred to as the striatal emotion processing network [EPN]) are conserved across species. We used the relationship between the EPN and projections from the anterior cingulate cortex (ACC) and orbitofrontal cortex (OFC) to assess network similarities across rats and monkeys.
We first compared the location and extent of each major component of the EPN in rats and macaques. Next, we used anatomic cases with anterograde injections in ACC/OFC to determine the extent to which corticostriatal terminal fields overlapped with these components and with each other.
The location and size of each component of the EPN were similar across species, containing projections primarily from infralimbic cortex in rats and area 25 in monkeys. Other ACC/OFC terminals overlapped extensively with infralimbic cortex/area 25 projections, supporting cross-species similarities in OFC topography. However, dorsal ACC had different connectivity profiles across species. These results were used to segment the monkey and rat striata according to ACC/OFC inputs.
Based on connectivity with the EPN, and consistent with prior literature, the infralimbic cortex and area 25 are likely homologues. We also see evidence of OFC homologies. Along with segmenting the striatum and identifying striatal hubs of overlapping inputs, these results help to translate findings between rodent models and human pathology.
Contrasting changes in extracellular dopamine and glutamate along the rostrocaudal axis of the anterior cingulate cortex of the rat following an acute d-amphetamine or dopamine challenge
2014, Neuropharmacology
Citation Excerpt :
The Cg1/Cg2 regions of the ACC are innervated by dopaminergic neurones from both the A10 and A9 nuclei, but their distribution differs in superficial (mainly A9) and deep layers (mainly A10). By contrast, the prelimbic region is innervated by neurones projecting from A10, only (Emson and Koob, 1978; Lindvall et al., 1978; Swanson, 1982; Berger et al., 1985; Zeng and Stuesse, 1991). These two groups of neurones differ in a number of respects, such as: the extent of their collateralisation (Loughlin and Fallon, 1984), expression of dopamine transporters (greater in Cg1 than in Cg2 and prelimbic cortex: Freed et al., 1995; Sesack et al., 1998) and co-storage of neurotensin (Febvret et al., 1991).
There is evidence for functional specificity of subregions along the rostrocaudal axis of the anterior cingulate cortex (ACC). The subregion-specific distribution of dopaminergic afferents and glutamatergic efferents along the ACC make these obvious candidates for coding such regional responses. We investigated this possibility using microdialysis in freely-moving rats to compare changes in extracellular dopamine and glutamate in the rostral (‘rACC’: Cg1 and Cg3 (prelimbic area)) and caudal (‘cACC’: Cg1 and Cg2) ACC induced by systemic or local administration of d-amphetamine. Systemic administration of d-amphetamine (3 mg/kg, i.p.) caused a transient increase in extracellular dopamine in the rACC, but an apparent increase in the cACC of the same animals was less clearly defined. Local infusion of d-amphetamine increased dopamine efflux in the rACC, only. Glutamate efflux in the rACC was increased by local infusion of dopamine (5–50 μM), which had negligible effect in the cACC, but only systemic administration of d-amphetamine increased glutamate efflux and only in the cACC. The asymmetry in the neurochemical responses within the rACC and cACC, to the same experimental challenges, could help explain why different subregions are recruited in the response to specific environmental and somatosensory stimuli and should be taken into account when studying the regulation of neurotransmission in the ACC.
This article is part of the Special Issue entitled ‘CNS Stimulants’.
Changes in synaptic efficacy of dentate granule cells during operant behavior in rats
2012, Physiology and Behavior
It is widely accepted that long-term potentiation (LTP) is one of the fundamental physiological mechanisms underlying memory function based on its response properties and behavior of the induced sites. Many experimental approaches have been used to investigate whether the mechanisms underlying LTP are activated during learning and whether these mechanisms underlie the formation of certain types of memory. However, relatively few studies have reported the time course of changes in the efficacy of synaptic transmission in the learning process. We simultaneously monitored changes in slope of field EPSPs (fEPSP slope) and the amplitude of population spikes (pop. spike) in perforant path-evoked potentials in the dentate gyrus over the course of an appetitively motivated operant paradigm in freely moving rats. We found that the fEPSP slope recorded from the granule cell layer was potentiated about 7%, the fEPSP slope recorded from the molecular layer was depressed about 20%, and the amplitude of pop. spike recorded from the granule cell layer was significantly depressed about 40% after the trial in which rats began to press the lever frequently. These results suggested that the granule cells in the dentate gyrus received excitatory inputs in the somatic region and inhibitory inputs in the dendritic region, and that outputs from the granule cells were significantly reduced in the process of acquisition of the operant behavioral task. We observed no LTP in this study although our rats were capable of having LTP induced by a high-frequency stimulus. The depression of fEPSP slope induced without any artificial stimulation in this study is thought to be another neural mechanism underlying learning and memory. The origins of excitatory and inhibitory inputs are unknown at the moment.
Effect of reversible inactivation of reuniens nucleus on memory processing in passive avoidance task
2011, Behavioural Brain Research
Citation Excerpt :
Pretraining bilateral hippocampal lesions showed a decrease in avoidance response retention evaluated 3 h posttraining [32]. Also, bilateral lesions of the medial prefrontal cortex resulted in loss of both fear and aggression in monkeys [41]. Fritts et al. reported that lesions to medial prefrontal cortex that spared the prelimbic area led to moderate deficits in shuttle-box avoidance [13].
The reuniens nucleus (RE) is the largest nucleus of the midline thalamic nuclei (MLN). RE has strongly connections with the amygdala and hippocampus, the structures that are involved in the learning and memory processes. In our previous report we have shown the role of RE in the spatial learning and memory using Morris water maze (MWM) task. Since RE is connected to multiple limbic structures, its involvement in the emotional learning and memory is a possibility. The present study was designed to elucidate the role of RE in acquisition, consolidation, and retrieval on the passive avoidance (PA) task which depends on a distributed network including the thalamus, amygdala, medial prefrontal cortex (mPFC) and hippocampus. For this purpose, rats were chronically implanted with a cannula aimed at the RE through which 0.5 μl tetracaine (2%) or saline were injected. Rats were trained in a PA task and their retention test was performed 24 h later. The injection of saline or tetracaine was applied 5 min before or 5, 90, and 360 min after the acquisition trial and 5 min before the retention tests. Our findings showed that inactivation of RE before training did not affect acquisition, but affected memory retention 24 h later in PA task. Moreover, inactivation of RE only 5 min after training impaired consolidation but not after 90 or 360 min. Also, inactivation of the RE, 5 min before the retrieval test impaired memory retrieval in PA task. In conclusion, it seems that RE is involved in memory processes in rats.
Regional variability in age-related loss of neurons from the primary visual cortex and medial prefrontal cortex of male and female rats
2008, Brain Research
Citation Excerpt :
Medial prefrontal cortex data from the adult group have been previously reported in Markham, Morris, and Juraska (2007). The mPFC was divided into the dorsal (anterior cingulate cortex, both dorsal and ventral regions: ACd and ACv) and ventral (prelimbic (PL) and infralimbic (IL)) regions based on differential afferent/efferent connections (Zeng and Stuesse, 1991; Verwer et al., 1996; Fisk and Wyss, 1999) and behavioral functions (Ragozzino and Rozman, 2007; Ragozzino et al., 2003). These two major regions were parcellated according to cytoarchitectonic criteria (Krettek and Price, 1977; Van Eden and Uylings, 1985) at 31.25× using a camera lucida (Figs. 1 and 2).
During aging, changes in the structure of the cerebral cortex of the rat have been seen, but potential changes in neuron number remain largely unexplored. In the present study, stereological methods were used to examine neuron number in the medial prefrontal cortex and primary visual cortex of young adult (85–90 days of age) and aged (19–22 months old) male and female rats in order to investigate any age-related losses. Possible sex differences in aging were also examined since sexually dimorphic patterns of aging have been seen in other measures. An age-related loss of neurons (18–20%), which was mirrored in volume losses, was found to occur in the primary visual cortex in both sexes in all layers except IV. Males, but not females, also lost neurons (15%) from layer V/VI of the ventral medial prefrontal cortex and showed an overall decrease in volume of this region. In contrast, dorsal medial prefrontal cortex showed no age-related changes. The effects of aging clearly differ among regions of the rat brain and to some degree, between the sexes.

View all citing articles on Scopus

View full text

Research reportMorphological heterogeneity within the cingulate cortex in rat: a horseradish peroxidase transport study

Abstract

Neurosci. Lett.

Brain Research

Brain Research

Brain Research

Brain Research

Brain Research

Neuropsychology

Behav. Neurol. Biol.

Brain Research

Brain Research

Brain Res. Rev.

Neurosci. Lett.

Neurosci. Lett.

Brain Research

Brain Research

Brain Res. Bull.

Neurosci. Lett.

Brain Research

Brain Research

Neurosci. Lett.

Stimulation in prefrontal cortex area inhibits cardiovascular and motor components of the defence reaction in rats

J. Auton. Nerv. Syst.

Convergent thalamic and mesencephalic projections to the anterior medial cortex in the rat

J. Comp. Neurol.

An autoradiographic examination of corticocortical and subcortical projections of the mediodorsal-projection (prefrontal) cortex of the rat

J. Comp. Neurol.

The motor cortex of the rat: cytoarchitecture and microstimulation mapping

J. Comp. Neurol.

Anatomical and electrophysiological evidence for a direct projection from Ammon's horn to the medial prefrontal cortex in the rat

Exp. Brain Res.

Research report
Morphological heterogeneity within the cingulate cortex in rat: a horseradish peroxidase transport study