Cue-sampling and goal-approach correlates of hippocampal unit activity in rats performing an odor-discrimination task

Several techniques previously used to describe behavioral correlates of hippocampal unit and slow-wave activity are combined in a single odor- discrimination paradigm. Rats repetitively performed a sequence of behaviors during each trial: approach to a stimulus-sampling port, investigatory sniffing of the odor cue, orientation and approach toward a separate reward location, and water reward consumption. In a series of post hoc analyses, spike activity was time-locked to variations of each task event to uncover behavioral and physiological parameters that best synchronized unit firing. Three major categories of cells were identified: (1) “Cue-sampling” cells fired after onset of odor-cue sampling. Response magnitude was related to cue valence on both the current and past trials. (2) “Goal-approach” cells fired prior to arrival at either the odor-sampling port or reward cup. A number of sampling and approach cells also had place correlates. However, detailed analyses indicated that specific behaviors associated with increased firing reliably occurred at the same place. Unit activity was at least as well described by behavioral as spatial parameters. (3) “Theta” cells fired at high rates in strict relation to the ongoing limbic theta rhythm. This categorization suggests a functional organization of the hippocampus in which different cell types play complementary roles. Cue-sampling cells activated by discriminative stimuli during attentive fixations may be involved in comparing relative cue valence. Goal-approach cells may be involved in orientation movements for successive cue-sampling periods. Theta cells may provide synchronization of sensory acquisition during sampling, as well as in orientation movements during approach.

[1]  C. H. Vanderwolf,et al.  Limbic-diencephalic mechanisms of voluntary movement. , 1971, Psychological review.

[2]  Vanderwolf Ch Limbic-diencephalic mechanisms of voluntary movement. , 1971 .

[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]  James L Olds,et al.  Activity of units in the hippocampal circuit of the rat during differential classical conditioning. , 1973, Journal of comparative and physiological psychology.

[5]  J. Winson,et al.  Patterns of hippocampal theta rhythm in the freely moving rat. , 1974, Electroencephalography and clinical neurophysiology.

[6]  E. Keller Participation of medial pontine reticular formation in eye movement generation in monkey. , 1974, Journal of neurophysiology.

[7]  R. Hirsh The hippocampus and contextual retrieval of information from memory: a theory. , 1974, Behavioral biology.

[8]  H. Eichenbaum,et al.  Compact miniature microelectrode-telemetry system , 1977, Physiology & Behavior.

[9]  D. Olton,et al.  Spatial correlates of hippocampal unit activity , 1978, Experimental Neurology.

[10]  G. Lynch,et al.  Activity of dentate granule cells during learning: Differentiation of perforant path input , 1979, Brain Research.

[11]  J. O’Keefe A review of the hippocampal place cells , 1979, Progress in Neurobiology.

[12]  G. Handelmann,et al.  Hippocampus, space, and memory , 1979 .

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

[14]  John O'Keefe,et al.  On the trail of the hippocampal engram , 1980 .

[15]  Theodore W. Berger,et al.  Hippocampal substrate of classical conditioning , 1980 .

[16]  Richard Hirsh,et al.  The hippocampus, conditional operations, and cognition , 1980 .

[17]  G. Winocur The hippocampus and cue utilization , 1980 .

[18]  H. Eichenbaum,et al.  Temporal relationship between sniffing and the limbic theta rhythm during odor discrimination reversal learning , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[20]  J. Gray,et al.  Précis of The neuropsychology of anxiety: An enquiry into the functions of the septo-hippocampal system , 1982, Behavioral and Brain Sciences.

[21]  Phillip J. Best,et al.  Reliability of the relationship between hippocampal unit activity and sensory-behavioral events in the rat , 1982, Experimental Neurology.

[22]  R. F. Thompson,et al.  Single-unit analysis of different hippocampal cell types during classical conditioning of rabbit nictitating membrane response. , 1983, Journal of neurophysiology.

[23]  M. Goodale,et al.  Neural Mechanisms of Visual Orientation in Rodents: Targets Versus Places , 1983 .

[24]  L. Nadel,et al.  The medial temporal region and memory consolidation: A new hypothesis , 2014 .

[25]  D. Gaffan,et al.  Delayed Matching by Fornix-Transected Monkeys: The Sample, the Push and the Bait , 1984, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[26]  J. Kubie A driveable bundle of microwires for collecting single-unit data from freely-moving rats , 1984, Physiology & Behavior.

[27]  J. Rawlins,et al.  Associations across time: The hippocampus as a temporary memory store , 1985, Behavioral and Brain Sciences.

[28]  D. Gaffan,et al.  Hippocampus: memory, habit and voluntary movement. , 1985, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[29]  H. Niki,et al.  Hippocampal unit activity and delayed response in the monkey , 1985, Brain Research.

[30]  H. Eichenbaum,et al.  Extracellular neural recording with multichannel microelectrodes , 1986 .

[31]  H Eichenbaum,et al.  Normal olfactory discrimination learning set and facilitation of reversal learning after medial-temporal damage in rats: implications for an account of preserved learning abilities in amnesia , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  S A Deadwyler,et al.  Behavioral functions and hippocampal cell types: evidence for two nonoverlapping populations in the rat. , 1986, Journal of neurophysiology.

[33]  R. Hampson,et al.  Sequential dependencies regulate sensory evoked responses of single units in the rat hippocampus , 1987, Brain Research.