Spatial correlates of firing patterns of single cells in the subiculum of the freely moving rat

Hippocampal lesions cause spatial learning deficits, and single hippocampal cells show location-specific firing patterns, known as place fields. This suggests the hippocampus plays a critical role in navigation by providing an ongoing indication of the animal's momentary spatial location. One question that has received little attention is how this locational signal is used by downstream brain regions to orchestrate actual navigational behavior. As a first step, we have examined the spatial firing correlates of cells in the dorsal subiculum as rats navigate in an open-field, pellet-searching task. The subiculum is one of the few major output zones for the hippocampus, and it, in turn, projects to numerous other brain areas, each thought to be involved in various learning and memory functions. Most subicular cells showed a robust locational signal. The patterns observed were different from those in the hippocampus, however, in that cells tended to fire throughout much of the environment, but showed graded, location-related rate modulation, such that there were some localized regions of high firing and other regions with relatively low firing. There were slight quantitative differences between the proximal (adjacent to the hippocampus) and distal (farther from the hippocampus) subicular regions, with distal cells showing slightly higher average firing rates, spatial signaling, and firing field size. This was of interest since these two regions have different efferent connections. Examination of spike trains allowed classification of cells into bursting, nonbursting, and theta (putative interneuron) categories, and this is similar to subicular cell types identified in vitro. Interestingly, the bursting and nonbursting types did not differ detectably in spatial firing properties, suggesting that differences in intrinsic membrane properties do not necessitate differences in coding of environmental inputs. The results suggest that the subiculum transmits a robust, highly distributed spatial signal to each of its projection areas, and that this signal is transmitted in both a bursting and nonbursting mode.

[1]  J. O'Keefe,et al.  The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. , 1971, Brain research.

[2]  A. Hjorth-Simonsen,et al.  Some intrinsic connections of the hippocampus in the rat: An experimental analysis , 1973, The Journal of comparative neurology.

[3]  J. B. Ranck,et al.  Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats. I. Behavioral correlates and firing repertoires. , 1973, Experimental neurology.

[4]  L. Nadel,et al.  Fornix lesions selectively abolish place learning in the rat , 1975, Experimental Neurology.

[5]  J. B. Ranck,et al.  Localization and anatomical identification of theta and complex spike cells in dorsal hippocampal formation of rats , 1975, Experimental Neurology.

[6]  L. E. White,et al.  Postcommissural fornix: Origin and distribution in the rodent , 1975, Neuroscience Letters.

[7]  W. Cowan,et al.  Hippocampo-hypothalamic connections: origin in subicular cortex, not ammon's horn. , 1975, Science.

[8]  A. Siegel,et al.  The origin of fornix fibers which project to the mammillary bodies in the rat: a horseradish peroxidase study , 1975, Brain Research.

[9]  J. O’Keefe Place units in the hippocampus of the freely moving rat , 1976, Experimental Neurology.

[10]  O. Steward,et al.  Topographic organization of the projections from the entorhinal area to the hippocampal formation of the rat , 1976, The Journal of comparative neurology.

[11]  W. Cowan,et al.  An autoradiographic study of the organization of the efferet connections of the hippocampal formation in the rat , 1977, The Journal of comparative neurology.

[12]  A. Siegel,et al.  Efferent connections of the hippocampal formation in the rat , 1977, Brain Research.

[13]  A. Siegel,et al.  Thalamic projections of the hippocampal formation: Evidence for an alternate pathway involving the internal capsule , 1977, Brain Research.

[14]  G. V. Van Hoesen,et al.  Hippocampal efferents reach widespread areas of cerebral cortex and amygdala in the rhesus monkey. , 1977, Science.

[15]  A. Siegel,et al.  Subicular projections to the posterior cingulate cortex in rats , 1977, Experimental Neurology.

[16]  W. Cowan,et al.  An autoradiographic study of the organization of intrahippocampal association pathways in the rat , 1978, The Journal of comparative neurology.

[17]  F. Gage,et al.  Hippocampal connections and spatial discrimination , 1978, Brain Research.

[18]  M. T. Shipley,et al.  Projections from the subiculum to the deep layers of the lpsilateral presubicular and entorhinal cortices in the guinea pig , 1979, The Journal of comparative neurology.

[19]  R. Passingham The hippocampus as a cognitive map J. O'Keefe & L. Nadel, Oxford University Press, Oxford (1978). 570 pp., £25.00 , 1979, Neuroscience.

[20]  T. Babb,et al.  Neurophysiology of the caudally directed hippocampal efferent system in the rat: Projections to the subicular complex , 1980, Brain Research.

[21]  W. Cowan,et al.  Evidence for collateral projections by neurons in Ammon's horn, the dentate gyrus, and the subiculum: a multiple retrograde labeling study in the rat , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  T. Babb,et al.  Demonstration of caudally directed hippocampal efferents in the rat by intracellular injection of horseradish peroxidase , 1981, Brain Research.

[23]  R. Morris,et al.  Place navigation impaired in rats with hippocampal lesions , 1982, Nature.

[24]  R. Sutherland,et al.  A behavioural analysis of spatial localization following electrolytic, kainate- or colchicine-induced damage to the hippocampal formation in the rat , 1983, Behavioural Brain Research.

[25]  G. Lynch,et al.  Patterned stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation , 1986, Brain Research.

[26]  Nobuaki Tamamaki,et al.  Columnar organization in the subiculum formed by axon branches originating from single CA1 pyramidal neurons in the rat hippocampus , 1987, Brain Research.

[27]  J. B. Ranck,et al.  Spatial firing patterns of hippocampal complex-spike cells in a fixed environment , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  R. Muller,et al.  The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  P. Best,et al.  Place cells and silent cells in the hippocampus of freely-behaving rats , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  D. Amaral,et al.  Lesions of perirhinal and parahippocampal cortex that spare the amygdala and hippocampal formation produce severe memory impairment , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  R. Muller,et al.  Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  T. van Groen,et al.  The postsubicular cortex in the rat: characterization of the fourth region of the subicular cortex and its connections , 1990, Brain Research.

[33]  Nobuaki Tamamaki,et al.  Disposition of the slab‐like modules formed by axon branches originating from single CA1 pyramidal neurons in the rat hippocampus , 1990, The Journal of comparative neurology.

[34]  M. Gabriel,et al.  Functions of anterior and posterior cingulate cortex during avoidance learning in rabbits. , 1990, Progress in brain research.

[35]  B. McNaughton,et al.  Comparison of spatial and temporal characteristics of neuronal activity in sequential stages of hippocampal processing. , 1990, Progress in brain research.

[36]  R U Muller,et al.  Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[37]  M. Witter,et al.  Heterogeneity in the Dorsal Subiculum of the Rat. Distinct Neuronal Zones Project to Different Cortical and Subcortical Targets , 1990, The European journal of neuroscience.

[38]  D. Amaral,et al.  Organization of CA1 projections to the subiculum: A PHA‐L analysis in the rat , 1991, Hippocampus.

[39]  J. Taube,et al.  Lesions of the rat postsubiculum impair performance on spatial tasks. , 1992, Behavioral and neural biology.

[40]  D. Amaral,et al.  Lesions of the perirhinal and parahippocampal cortices in the monkey produce long-lasting memory impairment in the visual and tactual modalities , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[41]  R K Wong,et al.  Intrinsic properties and evoked responses of guinea pig subicular neurons in vitro. , 1993, Journal of neurophysiology.

[42]  L. Squire,et al.  Damage to the perirhinal cortex exacerbates memory impairment following lesions to the hippocampal formation , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.