Head-direction cells in the rat posterior cortex (original) (raw)
Abstract
We examined the behavioral modulation of head-directional information processing in neurons of the rat posterior cortices, including the medial prestriate (area Oc2M) and retrosplenial cortex (areas RSA and RSG). Single neurons were recorded in freely moving rats which were trained to perform a spatial working memory task on a radial-arm maze in a cue-controlled room. A dual-light-emitting diode (dual-LED) recording headstage, mounted on the animals' heads, was used to track head position and orientation. Planar modes of motion, such as turns, straight motion, and nonlocomotive states, were categorized using an objective scheme based upon the differential contributions of movement parameters, including linear and angular velocity of the head. Of 662 neurons recorded from the posterior cortices, 41 head-direction (HD) cells were identified based on the criterion of maintained directional bias in the absence of visual cues or in the dark. HD cells constituted 7 of 257 (2.7%) cells recorded in Oc2M, 26 of 311 (8.4%) cells in RSA, and 8 of 94 (8.5%) cells in RSG. Spatial tuning of HD cell firing was modulated by the animal's behaviors in some neurons. The behavioral modulation occurred either at the preferred direction or at all directions. Moreover, the behavioral selectivity was more robust for turns than straight motions, suggesting that the angular movements may significantly contribute to the head-directional processing. These behaviorally selective HD cells were observed most frequently in Oc2M (4/7, 57%), as only 5 of 26 (19%) of RSA cells and none of the RSG cells showed behavioral modulation. These data, taken together with the anatomical evidence for a cascade of projections from Oc2M to RSA and thence to RSG, suggest that there may be a simple association between movement and head-directionality that serves to transform the egocentric movement representation in the neocortex into an allocentric directional representation in the periallocortex.
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References
- Albright TD, Desimone R, Gross CG (1984) Columnar organization of directionally selective cells in visual area MT of the macaque. J Neurophysiol 51:16–31
Google Scholar - Andersen RA (1987) Inferior parietal lobule function in spatial perception and visuomotor integration. In: Plum F (ed) Higher functions of the brain. (Handbook of physiology, sect 1, The nervous system, vol V, part 2) American Physiological Society, Bethesda, MD
Google Scholar - Andersen RA, Essick GK, Siegel RM (1985) Encoding of spatial location by posterior parietal neurons. Science 230:456–458
CAS PubMed Google Scholar - Andersen RA, Bracewell RM, Barach S, Gnadt JW, Fogassi L (1990) Eye position effect on visual, memory, and saccade-related activity in areas LIP and 7a of macaque. J Neurosci 10:1176–1196
Google Scholar - Chen LL, McNaughton BL (1988) Spatially selective discharge of vision and movement modulated posterior parietal neurons in the rat. Soc Neurosci Abstr 14:818
Google Scholar - Chen LL, McNaughton BL, Barnes CA, Ortiz ER (1990) Head-directional and behavioral correlates of posterior cingulate and medial prestriate cortex neurons in freely-moving rats. Soc Neurosci Abstr 16:441
Google Scholar - Chen LL, Lin L-H, McNaughton BL, Barnes CA, Gibbons DF (1991) Progressive decrease of behavioral modulation of head-direction cells from medial prestriate cortex to retrosplenial cortex. Soc Neurosci Abstr 17:1395
Google Scholar - Chen LL, Lin L-H, Barnes CA, McNaughton BL (1994) Head-direction cells in the rat posterior cortex. II. Contributions of visual and ideothetic information to the directional firing. Exp Brain Res 101:24–34
Google Scholar - Duhamel JR, Colby CL, Goldberg ME (1992) The updating of the representation of visual space in parietal cortex by intended eye movements. Science 255:90–92
Google Scholar - Eichenbaum H, Kuperstein M, Fagan A, Nagode J (1987) Cuesampling and goal-approach correlates of hippocampal unit activity in rats performing an odor-discrimination task. J Neurosci 7:716–732
Google Scholar - Gallistel CR (1990) The organization of learning. MIT press, Cambridge, MA
Google Scholar - Gallyas F (1979) Silver staining of myelin by means of physical development. Neurol Res 1:203–209
Google Scholar - Georgopoulos AP, Lurito JT, Petrides M, Schwartz AB, Massey JT (1989) Mental rotation of the neuronal population vector. Science 243:234–236
CAS PubMed Google Scholar - Groen T van, Wyss JM (1990a) The postsubicular cortex in the rat: characterization of the fourth region of the subicular cortex and its connections. Brain Res 529:165–177
Google Scholar - Groen T van, Wyss JM (1990b) Connections of the retrosplenial granular A cortex in the rat. J Comp Neurol 300:593–606
Google Scholar - Hyvarinen J (1982) The parietal cortex of monkey and man. Springer, Berlin Heidelberg New York
Google Scholar - Kolb B, Walkey J (1987) Behavioral and anatomical studies of the posterior parietal cortex in the rat. Behav Brain Res 23:127–145
Article CAS PubMed Google Scholar - Krieg WJS (1946) Connections of the cerebral cortex. I. The albino rat: A. Topography of the cortical areas. J Comp Neurol 84:221–275
Google Scholar - Mardia KV (1972) Statistics of directional data. Academic, New York
Google Scholar - McNaughton BL, Barnes CA, O'Keefe J (1983a) The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving rats. Exp Brain Res 52:41–49
CAS PubMed Google Scholar - McNaughton BL, O'Keefe J, Barnes CA (1983b) The stereotrode: a new technique for simultaneous isolation of several single units in the central nervous system from multiple unit records. J Neurosci Methods 8:391–397
Google Scholar - McNaughton BL, Green EJ, Mizumori SJY (1986) Representation of body-motion trajectory by rat sensory-motor cortex neurons. Soc Neurosci Abstr 12:260
Google Scholar - McNaughton BL, Chen LL, Marcus EJ (1991) “Dead Reckoning”, landmark learning, and the sense of direction: a neurophysiological and computational hypothesis. J Cogn Neurosci 3:190–202
Google Scholar - Mergner T, Siebold C, Schweigart G, Becker W (1991) Human perception of horizontal trunk and head rotation in space during vestibular and neck stimulation. Exp Brain Res 85:389–404
CAS PubMed Google Scholar - Miller MW, Vogt BA (1984) Direct connections of rat visual cortex with sensory, motor, and association cortices. J Comp Neurol 226:184–202
Google Scholar - Mittelstaedt ML, Mittelstaedt H (1980) Homing by path integration in a mammal. Naturwissenschaften 67:566
Google Scholar - Motter BC, Mountcastle VB (1981) The functional properties of the light-sensitive neurons of the posterior parietal cortex studied in walking monkeys: foveal sparing and opponent vector organization. J Neurosci 1:3–26
Google Scholar - Mountcastle VB, Lynch JC, Georgopoulos A, Sakata H, Acuna C (1975) Posterior parietal association cortex of the monkey: command function for operations with extrapersonal space. J Neurophysiol 38:871–908
Google Scholar - Muller RU, Kubie JL, Ranck JB (1987) Spatial firing patterns of hippocampal complex-spike cells in a fixed environment. J Neurosci 7:1935–1950
Google Scholar - Muller RU, Kubie JL, Bostock EM, Taube JS, Quirk GJ (1991) Spatial firing correlates of neurons in the hippocampal formation of freely moving rats. In: Paillard J (ed) Brain and space. Oxford University Press, Oxford, pp 296–333
Google Scholar - O'Keefe J (1979) A review of the hippocampal place cells. Prog Neurobiol 13:419–439
Article PubMed Google Scholar - O'Keefe J, Dostrovsky J (1971) The hippocampus as a spatial map: preliminary evidence from unit activity in the freely-moving rat. Brain Res 34:171–175
Google Scholar - Olton DS, Samuelson RJ (1976) Remembrance of places: spatial memory in rats. J Exp Psychol Anim Behav Process 2:97–116
Google Scholar - Potegal M (1987) The vestibular navigation hypothesis: a progress report. In: Ellen P, Thinus-Blanc C (eds) Cognitive processes and spatial orientation in animal and man, vol II. Nijhoff, Dordrecht
Google Scholar - Ranck JB (1984) Head-direction cells in the deep cell layer of dorsal presubiculum in freely moving rats. Soc Neurosci Abstr 10:599
Google Scholar - Robinson DA (1973) Models of the saccadic eye movement control system. Kybernetik 14:71–83
Google Scholar - Sparks DL, Mays LE (1990) Signal transformations required for the generation of saccadic eye movements. Annu Rev Neurosci 13:309–336
Google Scholar - Sripanidkulchai K, Wyss JM (1986) Thalamic projections of retrosplenial cortex in the rat. J Comp Neurol 254:143–165
Google Scholar - Taube JS, Muller RU, Ranck JB (1990a) Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J Neurosci 10:420–435
Google Scholar - Taube JS, Muller RU, Ranck JB (1990b) Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations. J Neurosci 10:436–447
Google Scholar - Toldi J, Foher O, Wolff JR (1986) Sensory interactive zones in the rat cerebral cortex. Neurosci 2:461–465
Google Scholar - Van Essen DC, Maunsell JHR, Bixby JL (1981) The temporal visual area in the macaque: myeloarchiteture, connections, functional properties and topographic connections. J Comp Neurol 199:293–326
Google Scholar - Vogt BA, Miller MW (1983) Cortical connections between rat cingulate cortex and visual, motor, and postsubicular cortices. J Comp Neurol 216:192–210
Google Scholar - Wieland CM, Eaton RC (1983) An electronic cine camera system for the automatic collection and analysis of high-speed movement of unrestrained animals. Behav Res Methods Instr 15:437–440
Google Scholar - Wiener SI (1993) Spatial and behavioral correlates of striatal neurons in rats performing a self-initiated navigational task. J Neurosci 13:3802–3817
Google Scholar - Wiener SI, Paul CA, Eichenbaum H (1989) Spatial and behavioral correlates of hippocampal neuronal activity. J Neurosci 9:2737–2763
Google Scholar - Zilles K (1985) The cortex of the rat: a stereotaxic atlas. Springer, Berlin Heidelberg New York
Google Scholar - Zipser D, Andersen RA (1988) A back-propagation programmed network that simulates response properties of a subset of posterior parietal neurons. Nature 331:679–684
Article CAS PubMed Google Scholar
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Author notes
- Longtang L. Chen
Present address: Laboratory for Neural Information, RIKEN 2-1, Hirosawa, 351-01, Saitama, Japan
Authors and Affiliations
- Behavioral Neuroscience Program, University of Colorado, 80309, Boulder, CO, USA
Longtang L. Chen, Lie-Huey Lin & Edward J. Green - ARL Division of Neural System, Memory and Aging, University of Arizona, 85724, Tucson, AZ, USA
Carol A. Barnes & Bruce L. McNaughton
Authors
- Longtang L. Chen
- Lie-Huey Lin
- Edward J. Green
- Carol A. Barnes
- Bruce L. McNaughton
Additional information
Laboratory of Neurogenetics, NIAAA, 12501 Washington Ave, Rockville, MD 20852; USA
Department of Psychology, University of Miami, Coral Gables, FL 33146, USA
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Chen, L.L., Lin, LH., Green, E.J. et al. Head-direction cells in the rat posterior cortex.Exp Brain Res 101, 8–23 (1994). https://doi.org/10.1007/BF00243212
- Received: 04 January 1993
- Accepted: 01 February 1994
- Issue date: September 1994
- DOI: https://doi.org/10.1007/BF00243212