Cortically projecting cells in the periaqueductal gray matter of the rat. A retrograde fluorescent tracer study
Abstract
The topographical organization of the afferent input from the periaqueductal gray matter (PAG) to the cerebral cortex has been assessed in rats by retrograde transport of the fluorescent tracers Fast blue (FB) and Diamidino yellow (DY). The olfactory, medial frontal (infralimbic, prelimbic and anterior cingulate cortices), lateral frontal (motor), parietal, temporal, occipital and insular cortices were explored by placing two fluorescent tracers into two different cortical regions. The PAG contained the largest number of labeled neurons in medial frontal cortex injections, followed by olfactory and lateral frontal cortices. Fewer retrogradely labeled cells were seen after injections in parietal, temporal occipital and insular cortices. All labeled cells were exclusively located in the medial and lateroventral divisions of the PAG (PAGm and PAGlv). The longitudinal extent of the labeling in PAGm was more extensive than in PAGlv. The labeled neurons in the medial frontal cortex group extended through most of the PAG, while in the remaining groups it was restricted to the caudal one-third of the PAG. Neurons with projections to two different cortical regions were only a small fraction of the total population of labeled cells. Our data indicate that the medial frontal cortex is the most important recipient of a direct PAG input, followed by the lateral frontal cortex. Parietal, temporal, occipital and insular cortices receive only a minor projection. It is concluded that the PAG sends direct projections over the majority of the cortical mantle. Therefore, the possibility arises that the cerebral cortex receives a direct influence from the brainstem without a thalamic relay.
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The periaqueductal gray sends monosynaptic reciprocal projections to ventromedial prefrontal cortex and to anterior mid-cingulate cortex, orbitofrontal cortex, and other areas involved in action value and defensive behavior.
“It also sends monosynaptic, reciprocal projections to the vmPFC—which is essential for value updating in the RL framework and likely for behavioral choice as well31—and to aMCC32, OFC and other areas involved in determining action value and coordinating defensive behavior18,33.”
From Representation of aversive prediction errors in the human periaqueductal gray (2014) · cites this paper as [32]
Cites
The rat brain in stereotaxic coordinates
Palkovits, M. (1983) · Neuropeptides · doi:10.1016/0143-4179(83)90049-5 · Cited by 28,959 · see citing works
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
Atlas of estradiol‐concentrating cells in the central nervous system of the female rat
Pfaff, D. W., & Keiner, M. (1973) · The Journal of Comparative Neurology · doi:10.1002/cne.901510204 · Cited by 1,494 · see citing works
Surgery in the Rat during Electrical Analgesia Induced by Focal Brain Stimulation
Reynolds, D. V. (1969) · Science · doi:10.1126/science.164.3878.444 · Cited by 1,380 · see citing works
Endogenous pain control mechanisms: Review and hypothesis
Basbaum, A. I., & Fields, H. L. (1978) · Annals of Neurology · doi:10.1002/ana.410040511 · Cited by 1,240 · see citing works
The entorhinal cortex of the monkey: II. Cortical afferents
Insausti, R., Amaral, D. G., & Cowan, W. M. (1987) · The Journal of Comparative Neurology · doi:10.1002/cne.902640306 · Cited by 835 · see citing works
Self-citationThe Cortex of the Rat: A Stereotaxic Atlas
Zilles, K. (1985) · Medical Entomology and Zoology · Cited by 657 · see citing works
The organization of afferent projections to the midbrain periaqueductal gray of the rat
Beitz, A. J. (1982) · Neuroscience · doi:10.1016/0306-4522(82)90157-9 · Cited by 544 · see citing works
Behavioral and electrophysiological evidence of pain inhibition from midbrain stimulation in the cat
Oliveras, J. L., Besson, J., Guilbaud, G., & Liebeskind, J. C. (1974) · Experimental Brain Research · doi:10.1007/bf00239016 · Cited by 420 · see citing works
Kuypers, H. G. J. M., Bentivoglio, M., Catsman‐Berrevoets, C. E., & Bharos, A. T. (1980) · Experimental Brain Research · doi:10.1007/bf00236147 · Cited by 406 · see citing works
Keizer, K., Kuypers, H. G. J. M., HUISMAN, A. M., & Dann, O. (1983) · Experimental Brain Research · doi:10.1007/bf00237193 · Cited by 348 · see citing works
Role of the periaqueductal grey in vocal expression of emotion
Jürgens, U., & Pratt, R. (1979) · Brain Research · doi:10.1016/0006-8993(79)90830-8 · Cited by 338 · see citing works
Connections of midbrain periaqueductal gray in the monkey. II. Descending efferent projections
Mantyh, P. W. (1983) · Journal of Neurophysiology · doi:10.1152/jn.1983.49.3.582 · Cited by 331 · see citing works
Organization of raphe-cortical projections in rat: A quantitative retrograde study
O’Hearn, E., & Molliver, M. E. (1984) · Brain Research Bulletin · doi:10.1016/0361-9230(84)90232-6 · Cited by 247 · see citing works
Lewis, V. A., & Gebhart, G. F. (1977) · Brain Research · doi:10.1016/0006-8993(77)90886-1 · Cited by 245 · see citing works
Subcortical electrical stimulation for control of intractable pain in humans
Hosobuchi, Y. (1986) · Journal of neurosurgery · doi:10.3171/jns.1986.64.4.0543 · Cited by 237 · see citing works
Stimulation of Periaqueductal Gray and Hypothalamus
Skultety, F. M. (1963) · Archives of Neurology · doi:10.1001/archneur.1963.00460060038004 · Cited by 216 · see citing works
The entorhinal cortex of the monkey: III. Subcortical afferents
Insausti, R., Amaral, D. G., & Cowan, W. M. (1987) · The Journal of Comparative Neurology · doi:10.1002/cne.902640307 · Cited by 214 · see citing works
Self-citationConnections of midbrain periaqueductal gray in the monkey. I. Ascending efferent projections
Mantyh, P. W. (1983) · Journal of Neurophysiology · doi:10.1152/jn.1983.49.3.567 · Cited by 169 · see citing works
Steinbusch, H. W. M., Nieuwenhuys, R., Verhofstad, A. A. J., & Van der Kooy, D. (1981) · PubMed · Cited by 165 · see citing works
Fardin, V., Oliveras, J. L., & Besson, J. (1984) · Brain Research · doi:10.1016/0006-8993(84)90361-5 · Cited by 161 · see citing works
Chi, C. C. (1970) · The Journal of Comparative Neurology · doi:10.1002/cne.901390302 · Cited by 153 · see citing works
Beitz, A. J. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902370403 · Cited by 147 · see citing works
Connexions of the dorsal tegmental nucleus in rat and rabbit.
Morest, D. K. (1961) · PubMed · Cited by 142 · see citing works
Efferent connections of the periaqueductal gray matter in the cat
Hamilton, B. L., & Skultety, F. M. (1970) · The Journal of Comparative Neurology · doi:10.1002/cne.901390107 · Cited by 138 · see citing works
Waterhouse, B. D., Mihailoff, G. A., Baack, J. C., & Woodward, D. J. (1986) · Journal of Comparative Neurology · doi:10.1002/cne.902490403 · Cited by 136 · see citing works
HUISMAN, A. M., Kuypers, H. G. J. M., & Verburgh, C. A. (1981) · Brain Research · doi:10.1016/0006-8993(81)90153-0 · Cited by 135 · see citing works
Hardy, S. G. P., & Leichnetz, G. R. (1981) · Neuroscience Letters · doi:10.1016/0304-3940(81)90183-x · Cited by 133 · see citing works
Eberhart, J. A., Morrell, J. I., Krieger, M. S., & Pfaff, D. W. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902410305 · Cited by 126 · see citing works
The midbrain periaqueductal gray in the rat, cat, and monkey: A Nissl, Weil, and Golgi analysis
Mantyh, P. W. (1982) · The Journal of Comparative Neurology · doi:10.1002/cne.902040406 · Cited by 122 · see citing works
de Olmos, J. S., & Heimer, L. (1980) · Neuroscience Letters · doi:10.1016/0304-3940(80)90247-5 · Cited by 118 · see citing works
Reichling, D. B., Kwiat, G. C., & Basbaum, A. I. (1988) · Progress in brain research · doi:10.1016/s0079-6123(08)62777-6 · Cited by 113 · see citing works
An air pressure system for the injection of tracer substances into the brain
Amaral, D. G., & Price, J. L. (1983) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(83)90107-3 · Cited by 111 · see citing works
Cytoarchitectural subdivisions of the periaqueductal gray matter in the cat
Hamilton, B. L. (1973) · The Journal of Comparative Neurology · doi:10.1002/cne.901490102 · Cited by 103 · see citing works
Depaulis, A., Bandler, R. J., & Vergnes, M. (1989) · Brain Research · doi:10.1016/0006-8993(89)91284-5 · Cited by 99 · see citing works
Hardy, S. G. P., & Leichnetz, G. R. (1981) · Neuroscience Letters · doi:10.1016/0304-3940(81)90070-7 · Cited by 96 · see citing works
The midbrain periaqueductal gray in the rat. II. A Golgi analysis
Beitz, A. J., & Shepard, R. D. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902370404 · Cited by 83 · see citing works
Neurons of the periaqueductal gray matter as revealed by Golgi study
Liu, R. P. C., & Hamilton, B. L. (1980) · The Journal of Comparative Neurology · doi:10.1002/cne.901890212 · Cited by 78 · see citing works
Brain stem neurons projecting to neocortex: A HRP study in the cat
Bentivoglio, M., Macchi, G., Rossini, P. M., & Tempesta, E. (1978) · Experimental Brain Research · doi:10.1007/bf00239807 · Cited by 61 · see citing works
Mobbs, C. V., Harlan, R., Burrous, M., et al. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-01-00113.1988 · Cited by 49 · see citing works
Bandler, R. J., & McCulloch, T. J. (1984) · Behavioural Brain Research · doi:10.1016/0166-4328(84)90171-2 · Cited by 47 · see citing works
McDougall, A., Dampney, R. A. L., & Bandler, R. J. (1985) · Neuroscience Letters · doi:10.1016/0304-3940(85)90383-0 · Cited by 45 · see citing works
Spinal neuronal collaterals to the intralaminar thalamic nuclei and periaqueductal gray
Liu, R. P. C. (1986) · Brain Research · doi:10.1016/0006-8993(86)90731-6 · Cited by 42 · see citing works
Andersen, E. (1986) · Brain Research · doi:10.1016/0006-8993(86)90955-8 · Cited by 40 · see citing works
Comparative cytoarchitectonic study of gudden's tegmental nuclei in some mammals
Hayakawa, T., & Zyo, K. (1983) · The Journal of Comparative Neurology · doi:10.1002/cne.902160302 · Cited by 38 · see citing works
Cytoarchitecture of the Periaqueductal Gray Matter in the Cat: A Quantitative Nissl Study
Gioia, M., Bianchi, R., & Tredici, G. (1984) · Cells Tissues Organs · doi:10.1159/000145870 · Cited by 35 · see citing works
Bandler, R. J., McCulloch, T. J., & Dreher, B. (1985) · Brain Research · doi:10.1016/0006-8993(85)90011-3 · Cited by 34 · see citing works
Moss, M. S., & Basbaum, A. I. (1983) · Brain Research · doi:10.1016/0006-8993(83)90004-5 · Cited by 33 · see citing works
Limbic influence on the periaqueductal gray: A single unit study in the awake squirrel monkey
Sandrew, B. B., & Poletti, C. E. (1984) · Brain Research · doi:10.1016/0006-8993(84)90212-9 · Cited by 24 · see citing works
Uptake of the retrograde fluorescent tracer Fast blue from the cerebrospinal fluid of the rat
Eisenman, L. M. (1985) · Neuroscience Letters · doi:10.1016/0304-3940(85)90584-1 · Cited by 15 · see citing works
Stimulation of the Periaqueductal Gray and Hypothalamus
(1963) · JAMA · doi:10.1001/jama.1963.03700250138055 · Cited by 5 · see citing works
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- Authors
- Herrero, M. T., Insausti, R., & Gonzalo, L. M.
- Affiliations
- Universidad de Navarra (ES)
- Corresponding author
- Herrero, M.T.
- Insausti, R.
- Venue
- Brain Research
- Publisher
- Elsevier BV
- Published
- 1991-03
- Volume
- 543
- Issue
- 2
- Pages
- 201-212
- ISSN
- 0006-8993 (ISSN-L)
- OpenAlex
- W2058048052
- Cited by
- 33
- References
- 51
- Citations by year
- 2026: 1 · 2024: 4 · 2020: 1 · 2019: 3 · 2018: 1 · 2017: 2 · 2016: 2 · 2015: 1 · 2014: 2 · 2013: 1
- FWCI
- 0.52
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Brain Research (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Health Sciences › Medicine › Physiology › Pain Mechanisms and Treatments
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- periaqueductal gray, corticopontine projections, medial frontal cortex, olfactory cortex, lateral frontal cortex, parietal cortex, temporal cortex, occipital cortex, insula, Fast Blue, Diamidino Yellow, retrograde tracing
- MeSH terms
- Animals, Cerebral Cortex, Female, Fluorescent Dyes, Frontal Lobe, Male, Occipital Lobe, Olfactory Bulb, Parietal Lobe, Periaqueductal Gray, Rats, Inbred Strains, Temporal Lobe, Rats
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