The hippocampus and motivation revisited: appetite and activity

https://doi.org/10.1016/S0166-4328(01)00364-3Get rights and content

Abstract

After reviewing the available data regarding the various effects of manipulating (e.g. lesions, chemical or electrical stimulation) the hippocampal formation, Jarrard [30] concluded that this structure likely played a role in motivated behaviors, specifically in general behavioral activation and incentive motivation. Since that time there have been technical advances in lesion techniques and conceptual advances in theories of motivation and learning. Here, we present more recent data that demonstrates the effects of hippocampal lesions on general activity, the utilization of interoceptive state cues, ingestive behaviors, and appetitive responding. We critically evaluate several theories of hippocampal function that have been proposed to explain these data, including the hippocampus as an inhibitor of general activation, as a processor of energy state signals and as a mediator of reward valuation. Finally, we propose that these findings may also be accounted for based on a role for the hippocampus in the learned inhibition of appetitive behaviors. We conclude that, while the specific mechanism of hippocampal involvement may not yet be determined, it is clear that this structure is involved in food-related behaviors and we caution researchers to consider this as a possible confound in studies of learning and memory processes.

Introduction

An enormous amount of research has been devoted to specifying the role of the hippocampus in learning and memory functions [32], [48]. Much of this research has attempted to assess the type and degree of learning and memory impairment that occurs as a consequence of removing or damaging the hippocampus. However, it is also possible that the hippocampus is involved with behavioral control processes in addition to those that are dependent on learning and memory.

In an earlier review, Jarrard [30] reported that animals with hippocampal lesions have been found to exhibit increased activity relative to controls. These activity differences were sometimes reported to interact with deprivation state (e.g. increased activity occurs when food-deprived but not following a meal). In addition, Jarrard [30] discussed studies in which hippocampal damage was reported to alter pattern and duration of meals, and in some studies, lesions increased food intake. Increased consumption was also reported following electrical and chemical (e.g. norepinephrine) stimulation of the hippocampus. Furthermore, moderately food-deprived rats with hippocampal lesions showed increased bar-pressing for food and other behavioral effects consistent with a heightened level of motivation. Based on this review, Jarrard [30] concluded that, in addition to learning and memory, hippocampal damage might influence response perseveration, nonspecific behavioral activation, incentive motivation, hunger, and other motivational functions.

The purpose of the present paper is to summarize research performed in our laboratory and elsewhere that investigates hippocampal involvement in motivational processes, especially those related to the control of feeding and appetitive behavior. This work will update Jarrard's earlier review in several ways. First, with a few exceptions, the studies presented here used an ibotenate lesioning technique that is more selective than the techniques (mainly aspiration and electrolytic procedures) that were used in the studies reviewed by Jarrard [30]. Compared to earlier procedures, the ibotenate lesioning technique permits more complete damage to the hippocampus, while leaving extrahippocampal structures and fibers of passage intact [31]. Accordingly, the effects of ibotenate lesions on behavioral activity, feeding, hunger, and incentive-based motivation are less plausibly attributed to damage that occurs outside the hippocampus.

Secondly, compared to the time when Jarrard published his review, more is known about the brain structures and neural circuits that are involved with the regulatory control of intake. We will summarize current knowledge, focusing on anatomical connections between the hippocampus and neural systems that are thought to be important substrates of feeding behavior. In addition, the conceptual frameworks (e.g. drive theory, S–R learning theory) available to Jarrard [30] are now considered to be largely untenable or incomplete. Therefore, we will reinterpret the effects of hippocampal damage on activity and appetitive behavior within contemporary theoretical accounts of motivation and learning. Finally, although this review emphasizes the involvement of the hippocampus in the control eating and appetitive behavior that normally maintain energy balance, studies that examine presumably nonregulatory appetitive and consummatory behavior in animals that are not food-deprived are also discussed. It is hoped that the analysis presented here will apply to the role of the hippocampus in both regulatory and nonregulatory forms of feeding behavior.

Section snippets

The hippocampus and appetitive processes

Any assessment of the role of the hippocampus in the regulation of eating and appetitive behavior must take into account that the performance of these behaviors may depend on the operation of a number of complex mechanisms. A long-standing idea is that performance is modulated by internal ‘hunger’ or ‘satiety’ signals that are correlated with the status of an animal's bodily energy resources [49]. Work in this area is often devoted to identifying the metabolic or hormonal origins of these

What does the hippocampus do?

The data presented in this paper show that selectively removing the hippocampus has the effects of (a) disrupting discrimination performance based on learning about cues arising from hunger and satiety but not performance based on learning about auditory cues; (b) increasing behavioral activity in the home cage, but does not interfere with behavioral immobility (conditioned freezing) in an apparatus that was associated with shock; (c) increasing food contacts and meal frequency, but not total

The hippocampus and inhibition of appetitive behavior

Animals that seek out and consume food on one occasion will show little interest in that same food at other times. This is a fundamental aspect of the regulatory control of food intake. Davidson [15], [16] proposed that the decision to eat or refrain from eating is based on learning to anticipate the postingestive consequences of food intake. According to this model, when food is consumed under deprivation, a particular appetitive postingestive consequence is incurred and an excitatory

Conclusions

The studies discussed above make it clear that the hippocampus plays an important role in the control of behaviors related to food appetite. As suggested by Jarrard [30] in his earlier review, more general motivational processes may underlie the effects of the hippocampus in this domain. Indeed, the effects and hypotheses explored here may be applicable to other ‘motivationally significant’ USs or rewards. However, as most available studies on the effects of hippocampal damage have used food as

References (53)

  • S.P. Kelley et al.

    Effects of hippocampal damage on reward threshold and response rate during self-stimulation of the ventral tegmental area in the rat

    Behav. Brain Res.

    (1999)
  • S. Ritter

    Multiple metabolic controls of feeding

    Appetite

    (1994)
  • J.W. Unger et al.

    Insulin receptors in the central nervous system: localization, signaling mechanisms and functional aspects

    Prog. Neurobiol.

    (1991)
  • N.S. Verkhratsky

    Limbic control of endocrine glands in aged rats

    Exp. Gerontol.

    (1995)
  • B. Balleine

    Instrumental performance following a shift in primary motivation depends on incentive learning

    J. Exp. Psychol. Anim. Behav. Process.

    (1992)
  • B.W. Balleine et al.

    The role of incentive learning in instrumental outcome revaluation by sensory-specific satiety

    Anim. Learn. Behav.

    (1998)
  • S.C. Benoit et al.

    Pavlovian conditioning and extinction of context cues and punctate CSs in rats with ibotenate lesions of the hippocampus

    Psychobiology

    (1999)
  • K.C. Berridge et al.

    The mind of an addicted brain: sensitization of wanting versus liking

    Curr. Dir. Psychol. Sci.

    (1995)
  • H.-R. Berthoud

    An overview of neural pathways and networks involved in the control of food intake and selection

  • Bratt AM, Kelley SP, Knowles JP, Barrett J, Davis K, Davis M, Mittleman G. Long term modulation of the HPA axis by the...
  • Chan K-H, Morell JR, Jarrard LE, Davidson TL, submitted for...
  • P.G. Clifton et al.

    Little and often: behavior patterns following hippocampal lesions in rats

    Behav. Neurosci.

    (1998)
  • L.H. Corbit et al.

    The role of the hippocampus in instrumental conditioning

    J. Neurosci.

    (2000)
  • T.L. Davidson

    Learning about deprivation intensity stimuli

    Behav. Neurosci.

    (1987)
  • T.L. Davidson

    The nature and function of interoceptive signals to feed: toward integration of physiological and learning perspectives

    Psychol. Rev.

    (1993)
  • T.L. Davidson

    Hunger cues as modulatory stimuli

  • Cited by (127)

    • Construction of complex memories via parallel distributed cortical–subcortical iterative integration

      2022, Trends in Neurosciences
      Citation Excerpt :

      However, to later researchers, the role of the hippocampus in amnesia (particularly obvious in Henry Mollaison [38]) made the circuit appear more relevant to memory. However, memory versus emotion is a false dichotomy given that goals require both, and hippocampal damage alters emotion [39–41]. Indeed, the hippocampus is among the main structures controlling the level of stress (and other) hormones [42–44].

    • Lateral septum as a nexus for mood, motivation, and movement

      2021, Neuroscience and Biobehavioral Reviews
    • Hippocampus ghrelin receptor signaling promotes socially-mediated learned food preference

      2018, Neuropharmacology
      Citation Excerpt :

      Ghrelin readily crosses the blood brain barrier (Banks et al., 2002, 2008), and recent studies have identified central nervous system sites of action for ghrelin-mediated appetite and hyperphagia (Alvarez-Crespo et al., 2012; King et al., 2011; Schele et al., 2016; Skibicka et al., 2011, 2013; St-Onge et al., 2015). Among these various sites, the hippocampus, a brain region traditionally associated with learning and memory, has been identified as a site of importance in the higher-order control of feeding and energy balance (Benoit et al., 2010; Davidson et al., 2005, 2014; Kanoski, 2012; Kanoski and Grill, 2017; Parent et al., 2014; Tracy et al., 2001). Interestingly, ghrelin receptors are extensively expressed in the hippocampus, particularly in the ventral subregion (vHP) (Mani et al., 2014; Zigman et al., 2006).

    View all citing articles on Scopus
    View full text