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

Abstract

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 timelocked 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 cuesampling periods. Theta cells may provide synchronization of sensory acquisition during sampling, as well as in orientation movements during approach.Despite extensive investigations of the hippocampus, we have only a vague understanding of its global functional role and little insight into its fundamental organization for information coding. The hippocampus is many synapses away from both receptor and effector neurons, so it is perhaps not surprising that progress in clarifying the functional correlates of hippocampal neurons has lagged behind that of sensory and motor neurons,

The hippocampal debate: are we asking the right questions?

“…By this point, it is pretty much accepted that under certain conditions, hippocampal pyramidal cells show correlations to non-spatial aspects [48,69,71,101,109,157,238,239,246,247,250] (see [33,173] for reviews, but see [147] for an alternative viewpoint). These non-spatial aspects include when animals change task within an environment [101], in response to components of a task in which goals change [48,69,157,247], even after salient events [202].…”

“…These non-spatial aspects include when animals change task within an environment [101], in response to components of a task in which goals change [48,69,157,247], even after salient events [202]. In addition, hippocampal cells show place field changes with changes in environments or the available constellation of cues [17,90,93,129,148,181,219,223,250].…”

“…All non-spatial hippocampal correlates have been measured along categorized dimensions: specific odors [48,246], whether a cue is black or white [17], whether the goal is to the left or right of a T-maze [54,247], whether a lever is to the left or to the right [71], whether two sequential cues match or not [69,157,[193][194][195], which behavior is to be elicited [101], etc. In contrast, studies of spatial dimensions have shown conclusively that the representation changes continuously (e.g.…”

“…This happens when animals change environments [93,223], when animals reverse direction on repeated paths [101,109], when animals change task within an environment [101], in response to components of a task in which goals change [48,157,247], with changes in salient cues [17], and in response to incompatible cue manipulations [89,175,202,204,219].…”

Olfactory loss in alcoholics: Correlations with cortical and subcortical MRI indices

“…Ablation of the orbitofrontal region of both rats (9) and primates (34) is associated with deficits in olfactory discrimination. Hippocampal damage also compromises olfactory discrimination in rats, but only if the task includes the simultaneous presentation of two stimuli (5)(6)(7)26). Human studies have indicated that patients with focal brain lesions involving orbitofrontal (21,28,37) or anterior temporal cortex (8,10,21,30,37) are impaired on odor identification and discrimination tasks.…”