Elsevier

Cortex

Volume 62, January 2015, Pages 119-157
Cortex

Special issue: Review
Limbic systems for emotion and for memory, but no single limbic system

https://doi.org/10.1016/j.cortex.2013.12.005Get rights and content

Abstract

The concept of a (single) limbic system is shown to be outmoded. Instead, anatomical, neurophysiological, functional neuroimaging, and neuropsychological evidence is described that anterior limbic and related structures including the orbitofrontal cortex and amygdala are involved in emotion, reward valuation, and reward-related decision-making (but not memory), with the value representations transmitted to the anterior cingulate cortex for action–outcome learning. In this ‘emotion limbic system’ a computational principle is that feedforward pattern association networks learn associations from visual, olfactory and auditory stimuli, to primary reinforcers such as taste, touch, and pain. In primates including humans this learning can be very rapid and rule-based, with the orbitofrontal cortex overshadowing the amygdala in this learning important for social and emotional behaviour. Complementary evidence is described showing that the hippocampus and limbic structures to which it is connected including the posterior cingulate cortex and the fornix-mammillary body-anterior thalamus-posterior cingulate circuit are involved in episodic or event memory, but not emotion. This ‘hippocampal system’ receives information from neocortical areas about spatial location, and objects, and can rapidly associate this information together by the different computational principle of autoassociation in the CA3 region of the hippocampus involving feedback. The system can later recall the whole of this information in the CA3 region from any component, a feedback process, and can recall the information back to neocortical areas, again a feedback (to neocortex) recall process. Emotion can enter this memory system from the orbitofrontal cortex etc., and be recalled back to the orbitofrontal cortex etc. during memory recall, but the emotional and hippocampal networks or ‘limbic systems’ operate by different computational principles, and operate independently of each other except insofar as an emotional state or reward value attribute may be part of an episodic memory.

Introduction

The concept of the limbic system has a long history, and is a concept that has endured to the present day (Catani et al., 2013, Mesulam, 2000).

In this paper I describe evidence that there are separate systems in the brain for emotion and for memory, each involving limbic structures, but that there is no single limbic system. We might term the system for emotion the ‘emotional limbic system’, and the system for memory the ‘memory limbic system’, but there are non-limbic components to both systems. The important concept I advance here is that the systems for emotion and for episodic memory involve largely different brain structures and connections, and different computational principles of operation, which are described. I argue here that of course some links from the emotional system into the memory system are present, for often an emotional state is part of an episodic memory, and when that episodic memory is recalled, the emotional state must be included in what is recalled. These concepts are important not only within neuroscience, but also for neurology (Catani et al., 2013, Mesulam, 2000), neuropsychology (Aggleton, 2012), and psychiatry.

Section snippets

Historical background to the concept of a limbic system

The use of the term ‘limbic’ has changed over time, but the concept of a limbic system is still in use (Catani et al., 2013). The term ‘limbic’ was introduced by Thomas Willis (1664) to designate a cortical border encircling the brainstem (limbus, Latin for ‘border’). Paul Broca (1878) held the view that ‘le grand lobe limbique’ was mainly an olfactory structure common to all mammalian brains, although he argued that its functions were not limited to olfaction. Limbic structures are frequently

Emotions defined

A very useful working definition of emotions is that they are states elicited by rewards and punishers, that is, by instrumental reinforcers (Gray, 1975, Rolls, 2005, Rolls, 2014, Weiskrantz, 1968). Instrumental reinforcers are rewards and punishers that are obtained as a result of an action instrumental in gaining the reward or avoiding the punisher. This approach is supported by many considerations (Rolls, 2014), including the following three. First, the definition is conceptually acceptable,

A hippocampal limbic system for memory and spatial function

Evidence will be described that the hippocampus and its connected structures are involved in episodic memory, and not in emotion. This is thus a separate system from the amygdala/orbitofrontal cortex/ACC emotional system. Moreover, the computational principles of operation of these two systems are very different.

Different computations for the ‘emotional limbic system’ from those in the ‘memory limbic system’

The circuitry involved in emotion in primates is shown schematically in Fig. 1.

It is crucial that the representation of primary (unlearned) reinforcers becomes explicit, i.e., in terms of reward value, in the orbitofrontal cortex. In the case of taste, my hypothesis is that genetic encoding of pathways is used to implement this (Rolls, 2014), with molecular specification of the synapses in the pathways from the genetically encoded taste receptors (Chandrashekar et al., 2006, Chaudhari and

Conclusions: separate limbic structures or systems for emotion and for memory, but no single limbic system

The concept of a (single) limbic system has been shown to be outmoded, in that anterior limbic and related structures involved in emotion can operate independently, and by different computational principles, from the hippocampal memory system. Instead, the anatomical, neurophysiological, functional neuroimaging, and neuropsychological evidence described shows that anterior limbic and related structures including the orbitofrontal cortex and amygdala are involved in emotion, reward valuation,

Acknowledgements

The author has worked on some of the investigations described here with I. De Araujo, G.C. Baylis, L.L. Baylis, A. Berthoz, A. Bilderbeck, M.C.A. Booth, R. Bowtell, A.D. Browning, H.D. Critchley, J.D. Feigenbaum, S. Francis, L. Franco, P. Georges-Francois, F. Grabenhorst, M.E. Hasselmo, C. Holscher, J. Hornak, M. Kadohisa, R.P. Kesner, M. Kringelbach, C.M. Leonard, C. Margot, C. McCabe, F. McGlone, F. Mora, J. O'Doherty, B.A. Parris, D.I. Perrett, J. Redoute, R.G. Robertson, M.K. Sanghera, T.R.

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