Cited by 101Neuroscience and Neuropharmacology ResearchMemory and Neural MechanismsNeural dynamics and brain function

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Morphological evidence that CA1 hippocampal afferents monosynaptically innervate PV-containing neurons and NADPH-diaphorase reactive cells in the medial prefrontal cortex (Areas 25/32) of the rat

Gabbott, Paul, Headlam, Anthony, Busby, Sarah·2002·Brain Research

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Abstract

Immunocytochemical and ultrastructural evidence is presented indicating that direct inputs from the hippocampal CA1 field to prelimbic (area 32) and infralimbic (area 25) cortices in the rat, innervate not only 'spiny' (presumed pyramidal) neurons but also monosynaptically contact NADPH-diaphorase reactive cells and parvalbumin-containing local circuit neurons-the latter cell type is shown to be GABA immunoreactive. Similar evidence of direct CA1 input to local circuit neurons containing either calbindin or calretinin was not found.

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Background
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Background
Dopamine D5 receptor immunoreactivity is differentially distributed in GABAergic interneurons and pyramidal cells in the rat medial prefrontal cortex
Oda, S., Funato, H., Adachi‐Akahane, S., Ito, M., Okada, A., Igarashi, H., Yokofujita, J., & Kuroda, M. (2010) · Brain Research · doi:10.1016/j.brainres.2010.03.011 · Cited by 30
Cooperativity between hippocampal–prefrontal short-term plasticity through associative long-term potentiation
Kawashima, H., Izaki, Y., Grace, A. A., & Takita, M. (2006) · Brain Research · doi:10.1016/j.brainres.2006.06.034 · Cited by 30
Amygdala afferents monosynaptically innervate corticospinal neurons in rat medial prefrontal cortex
Gabbott, P. L. A., Warner, T., Brown, J. Y., Salway, P., Gabbott, T., & Busby, S. J. (2012) · The Journal of Comparative Neurology · doi:10.1002/cne.23047 · Cited by 29
“5B,C ), especially by using the correlated light/electron microscope procedure adopted here (Hussain et al., 1996; Gabbott et al., 2002, 2007).”
MethodInfluential
Functional structure of the intermediate and ventral hippocampo–prefrontal pathway in the prefrontal convergent system
Takita, M., Fujiwara, S.-E., & Izaki, Y. (2013) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2013.05.002 · Cited by 27
“1 (right panel) (Gabbott et al., 2002; Jay and Witter, 1991; Swanson, 1981).”
Background
Amyloid β Peptide-Induced Changes in Prefrontal Cortex Activity and Its Response to Hippocampal Input
Flores-Martínez, E., & Peña‐Ortega, F. (2017) · International Journal of Peptides · doi:10.1155/2017/7386809 · Cited by 26
Long-term potentiation prevents ketamine-induced aberrant neurophysiological dynamics in the hippocampus-prefrontal cortex pathway in vivo
Lopes‐Aguiar, C., Ruggiero, R. N., Rossignoli, M. T., Esteves, I. D. M., Peixoto-Santos, J. E., Romcy-Pereira, R. N., & Leite, J. P. (2020) · Scientific Reports · doi:10.1038/s41598-020-63979-5 · Cited by 21
Distinctive morphology of hippocampal CA1 terminations in orbital and medial frontal cortex in macaque monkeys
Zhong, Y.-M., Yukie, M., & Rockland, K. (2006) · Experimental Brain Research · doi:10.1007/s00221-005-0187-7 · Cited by 26
Dopamine D1 receptor in the medial prefrontal cortex mediates anxiety-like behaviors induced by blocking glutamatergic activity of the ventral hippocampus in rats
Liu, L., Zhang, L., Wang, T., & Chen, L. (2018) · Brain Research · doi:10.1016/j.brainres.2018.09.024 · Cited by 25
Maturation of Corticolimbic Functional Connectivity During Sensitive Periods of Brain Development
Yang, S., & Tseng, K. Y. (2021) · Current topics in behavioral neurosciences · doi:10.1007/7854_2021_239 · Cited by 22
Afferent Drive of Medial Prefrontal Cortex by Hippocampus and Amygdala is Altered in MAM-Treated Rats: Evidence for Interneuron Dysfunction
Esmaeili, B., & Grace, A. A. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.64 · Cited by 22
Catecholaminergic neurons in medullary nuclei are among the post-synaptic targets of descending projections from infralimbic area 25 of the rat medial prefrontal cortex
Gabbott, P. L. A., Warner, T., & Busby, S. J. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.09.048 · Cited by 21
“In comparison, TH-immunoreactive structures labeled using Vector SG contained a distinctive granular reaction endproduct embedded in a fine diffuse background label (Hussain et al., 1996; Gabbott et al., 2002).”
BackgroundMethod
Entorhinal Cortex Inhibits Medial Prefrontal Cortex and Modulates the Activity States of Electrophysiologically Characterized Pyramidal Neurons In Vivo
Valenti, O., & Grace, A. A. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhn114 · Cited by 21
“In an ultrastructural study, CA1 hippocampal afferents to the mPFC were shown to innervate parvalbumin-containing neurons as well as pyramidal neurons (Gabbott et al. 2002).”
In vivo temporal property of GABAergic neural transmission in collateral feed-forward inhibition system of hippocampal–prefrontal pathway
Takita, M., Kuramochi, M., Izaki, Y., & Ohtomi, M. (2007) · Brain Research · doi:10.1016/j.brainres.2007.02.063 · Cited by 21
Ventral hippocampal projections to infralimbic cortex and basolateral amygdala are differentially activated by contextual fear and extinction recall
Brockway, E. T., Simon, S., & Drew, M. R. (2023) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2023.107832 · Cited by 26
Points of divergence on a bumpy road: early development of brain and immune threat processing systems following postnatal adversity
Brenhouse, H. C. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01658-9 · Cited by 20
Neural Plasticity Is Involved in Physiological Sleep, Depressive Sleep Disturbances, and Antidepressant Treatments
Zhang, M., Li, R., Wang, Y., & Huang, Z. (2017) · Neural Plasticity · doi:10.1155/2017/5870735 · Cited by 19
“In addition, pyramidal cells and interneurons in the medial prefrontal cortex (mPFC) can be excited by CA1 pyramidal cells from the ventral part of the hippocampus [37], and the amygdala complex, which is a critical interface for emotional responses, is reciprocally connected with the regions that are implicated in th…”
Background
Activation of α7 nicotinic acetylcholine receptors facilitates long-term potentiation at the hippocampal-prefrontal cortex synapses in vivo
Stoiljković, M., Kelley, C., Nagy, D., Hurst, R. S., & Hajós, M. (2016) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2016.11.003 · Cited by 20
Human Brain Oscillations: From Physiological Mechanisms to Analysis and Cognition
Jensen, O. B., Spaak, E., & Zumer, J. M. (2019) · Springer eBooks · doi:10.1007/978-3-030-00087-5_17 · Cited by 22
Evidence for Competition for Target Innervation in the Medial Prefrontal Cortex
Guirado, R., Umemori, J., Sipilä, P., & Ċastrén, E. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhv280 · Cited by 21
“Both projections have been reported to innervate both CAMKII-expressing pyramidal neurons and PV-expressing interneurons, as we observe here in our study (Carr and Sesack 1996; Gabbott et al. 2002, 2006).”
BackgroundResult
Differential regulation of glutamic acid decarboxylase gene expression after extinction of a recent memory vs. intermediate memoryPreprint
Sangha, S., Ilenseer, J., Sosulina, L., Lesting, J., & Pape, H. (2012) · Learning & Memory · doi:10.1101/lm.025874.112 · Cited by 17
“Thus, extinction of a recent memory resulted in reduced Gad65 gene expression in both the DG and CA1.”
Background
Hippocampal Theta Modulation of Neocortical Spike Times and Gamma Rhythm: A Biophysical Model Study
Spaak, E., Zeitler, M., & Gielen, S. C. A. M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0045688 · Cited by 14
“The projections to the interneurons, however, are stronger than those to the pyramidal cells [31,32].”
High frequency stimulation of the infralimbic cortex induces morphological changes in rat hippocampal neurons
Bezchlibnyk, Y. B., Stone, S. S. D., Hamani, C., & Lozano, A. M. (2016) · Brain stimulation · doi:10.1016/j.brs.2016.11.013 · Cited by 16
Monosynaptic Retrograde Tracing From Prelimbic Neuron Subpopulations Projecting to Either Nucleus Accumbens Core or Rostromedial Tegmental Nucleus
Cruz, A. M., Kim, T. H., & Smith, R. J. (2021) · Frontiers in Neural Circuits · doi:10.3389/fncir.2021.639733 · Cited by 14
“Extensive previous work has characterized inputs to both pyramidal neurons and interneurons in PL arising from the ventral hippocampus (Ferino et al., 1987; Jay et al., 1989, 1992; Jay and Witter, 1991; Condé et al., 1995; Carr and Sesack, 1996; Gabbott et al., 2002; Hoover and Vertes, 2007) and BLA (Bacon et al.”
Background
Synaptic plasticity dynamics in the hippocampal-prefrontal pathway in vivo
Takita, M., Izaki, Y., Kuramochi, M., Yokoi, H., & Ohtomi, M. (2009) · Neuroreport · doi:10.1097/wnr.0b013e3283344949 · Cited by 13
The anatomy of co-morbid neuropsychiatric disorders based on cortico-limbic synaptic interactions
Totterdell, S. (2006) · Neurotoxicity Research · doi:10.1007/bf03033236 · Cited by 13
Reversing neural circuit and behavior deficit in mice exposed to maternal inflammation by Zika virus
Ma, L., Wang, J., Ge, J., Wang, Y., Zhang, W., Du, Y., Luo, J., Li, Y., Wang, F., Fan, G., et al. (2021) · EMBO Reports · doi:10.15252/embr.202051978 · Cited by 9
“Pyramidal neurons in the vHIP send axonal projections to the mPFC, where they form mono-excitatory glutamatergic synapses with both excitatory and inhibitory neurons in the deep layers of mPFC (Thierry et al , 2000; Gabbott et al , 2002; Liu & Carter, 2018; Phillips et al , 2019).”
Coupling between the prelimbic cortex, nucleus reuniens, and hippocampus during NREM sleep remains stable under cognitive and homeostatic demands
Bozic, I., Rusterholz, T., Mikutta, C. A., Rio‐Bermudez, C. D., Nissen, C., & Adamantidis, A. (2022) · European Journal of Neuroscience · doi:10.1111/ejn.15853 · Cited by 10
“We stereotactically implanted male mice with multi-site electrodes in Nre, ventral and dorsal portion of CA1 (vCA1 and dCA1), and the prelimbic portion of the mPFC (Prl) on the left hemisphere.”
BackgroundInfluential
Hippocampal-Prefrontal Cortical Circuit and Working Memory
Wang, G.-W., & Cai, J. (2010) · Zoological Research · doi:10.3724/sp.j.1141.2010.00050 · Cited by 9
Dorsal–Caudal and Ventral Hippocampi Target Different Cell Populations in the Medial Frontal Cortex in Rodents
Alemán-Andrade, P., Witter, M. P., Tsutsui, K., & Ohara, S. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.0217-25.2025 · Cited by 9
Individualized frequency and montage tACS to engage theta-gamma coupling and enhance working memory in mild cognitive impairment
Mirjalili, M., Palamarchuk, I. S., Brooks, H., Zomorrodi, R., Melichercik, A., Wang, W., Nestor, S. M., Blumberger, D. M., Datta, A., Bowie, C. R., et al. (2025) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2025.1565881 · Cited by 8
Role of Neural Circuits in Cognitive Impairment
Zhang, L., Liu, G., Peng, Y., Gao, J., & Tian, M. (2024) · Neurochemical Research · doi:10.1007/s11064-024-04309-3 · Cited by 6
“These connections could control the excitatory state of pyramidal cells in the PFC at a certain level and prevent excessive excitation [206].”
Long‐range inputome of prefrontal GABAergic interneurons in the Alzheimer's disease mouse
Ren, M., Li, Y., Jiang, T., Liu, B., Li, X., Jia, X., Li, A., Luo, Q., Gong, H., & Li, X. (2025) · Alzheimer s & Dementia · doi:10.1002/alz.14552 · Cited by 5
“35 For example, both PV + and SOM + neurons receive input information from hippocampal pyramidal neurons; the former participates in social preference memory expression, whereas the latter participates in spatial working memory formation.”
Human Brain Oscillations: From Physiological Mechanisms to Analysis and Cognition
Jensen, O. B., Spaak, E., & Zumer, J. M. (2019) · Springer eBooks · doi:10.1007/978-3-319-62657-4_17-1 · Cited by 9
Up and Down Regulation of Synaptic Strength at Hippocampal to Prefrontal Cortex Synapses
Jay, T. M., Gurden, H., Rocher, C., Hotte, M., & Spedding, M. (2006) · Kluwer Academic Publishers eBooks · doi:10.1007/1-4020-7949-4_5 · Cited by 5
“Synaptic contacts are formed with dendritic spines from pyramidal neurons but also with dendritic shafts of local circuit GABA neurons ( Gabbott et al., 2002 ).”
Background
The Prefrontal Cortex: A Basic Embryological, Histological, Anatomical, and Functional Guideline
(2016) · Journal of Human Anatomy & Physiology · doi:10.13188/2575-7563.1000005 · Cited by 3
ГЕНЕРАЛИЗАЦИЯ СТРАХА В МОДЕЛЯХ НА ЖИВОТНЫХ: НЕЙРОФИЗИОЛОГИЧЕСКИЕ МЕХАНИЗМЫ И ВОЗМОЖНЫЕ МИШЕНИ КОРРЕКЦИИ, "Успехи физиологических наук"
Саульская, Н. Б. (2018) · Успехи физиологических наук · doi:10.7868/s0301179818040021 · Cited by 3
Mouse Medial-prefrontal Cortex Involvement in Trace Fear Memory during Wakefulness and Sleep
Steenland, H. W. (2011) · TSpace (University of Toronto) · Cited by 1
Distribuição de receptores ionotrópicos de glutamato e sua co-localização com a fosfoproteína neural DARPP-32 no córtex pré-frontal de ratos.
Sambé, N. A. (2009) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/t.42.2009.tde-22012010-100738
Behavioral, molecular and neurobiological processes underlying memory retrieval
Stafford, J. M. (2016) · doi:10.6083/m40k26kj
CIRCUIT DYNAMICS UNDERLYING CONTROL OF DOPAMINE NEURON ACTIVITY BY THE NUCLEUS REUNIENS OF THE MIDLINE THALAMUS
Zimmerman, E. I. (2017) · D-Scholarship@Pitt (University of Pittsburgh)
Nicotinic Signalling and Neurosteroid Modulation in Principal Neurons of the Hippocampal Formation and Prefrontal Cortex
Chung, B. Y. T. (2018) · The Atrium (University of Guelph)
Early life esophageal acid exposure reduces expression of NMDAR1 in the adult rat dorsal hippocampus and medial prefrontal cortex: Potential relationship with hyperlocomotion
Zhang, W., Wang, X., Wang, K., & Duan, L. (2018) · Journal of Digestive Diseases · doi:10.1111/1751-2980.12650
Loneliness, serotonin, and medial prefrontal cortex: some empirical and theoretical considerations
Fitzgerald, P. J. (2026) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2026.174189
Rôle des récepteurs 5-HT2A et 5-HT6 du cortex préfrontal dans la modulation de la transmission synaptique, la plasticité et la cognition
Berthoux, C. (2017) · theses.fr (ABES) · doi:10.70675/4a004943zc84ez4f85z80d7z47bd0c2b7848

Authors: Gabbott, P., Headlam, A., & Busby, S.
Affiliations: University of Oxford (GB)
Corresponding author: Gabbott, Paul
Venue: Brain Research
Publisher: Elsevier BV
Published: 2002-08
Volume: 946
Issue: 2
Pages: 314-322
ISSN: 0006-8993 (ISSN-L)
DOI: 10.1016/s0006-8993(02)02487-3
OpenAlex: W2111161101
Cited by: 101
References: 43
Citations by year: 2026: 1 · 2025: 3 · 2024: 1 · 2023: 1 · 2022: 2 · 2021: 5 · 2020: 8 · 2019: 5 · 2018: 7 · 2017: 6 · 2016: 7 · 2015: 2 · 2014: 8 · 2013: 6 · 2012: 4
FWCI: 1.39
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Brain Research (publishedVersion)
PubMed (publishedVersion)
Open Research Online (The Open University) (submittedVersion)
Funders: Wellcome Trust
Royal Society
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
Keywords: hippocampal CA1, medial prefrontal cortex, parvalbumin, NADPH-diaphorase, local circuit neurons, GABA immunoreactivity, calbindin, calretinin, pyramidal neurons
MeSH terms: Afferent Pathways, Animals, Electrophysiology, gamma-Aminobutyric Acid, Hippocampus, Immunohistochemistry, Limbic System, Male, NADPH Dehydrogenase, Neurons, Afferent, Parvalbumins, Synapses, Rats, Sprague-Dawley, Prefrontal Cortex, Rats, Calbindins, S100 Calcium Binding Protein G, Calbindin 2

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Morphological evidence that CA1 hippocampal afferents monosynaptically innervate PV-containing neurons and NADPH-diaphorase reactive cells in the medial prefrontal cortex (Areas 25/32) of the rat

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