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