ReviewParallel associative processing in the dorsal striatum: Segregation of stimulus–response and cognitive control subregions
Highlights
► A theory concerning the functional contributions of the dorsal striatum is presented. ► Anatomical, physiological, and behavioral data is reviewed to support this view. ► Dorso-lateral striatum is thought to be critical for stimulus–response learning. ► Dorso-medial striatum is thought to contribute to the cognitive control of behavior. ► Unanswered questions concerning the functions of these systems are explored.
Introduction
Ideas about basal ganglia function have historically shifted back and forth between sensory/cognitive views and motor/inhibitory accounts (Divac & Öberg, 1979). Early proposals noted the location of the basal ganglia near the cerebral ventricles, which were believed to be the location of the ‘mind’ since the time of Galen (∼199 A.D.) (Kolb & Whishaw, 1995). Consequently, complex cognitive functions such as thinking, memory and imagination were ascribed to the basal ganglia (Divac & Öberg, 1979). The English anatomist Thomas Willis (1664) noted that the corpus striatum received input from all sensory modalities, consistent with Aristotle’s ‘sensorium commune.’ Nearly a century later in 1740, Swedenborg declared that “the royal road of the sensations of the body to the soul is through the corpora striata and all determinations of the will also descend by that route” (as cited in Iversen, 1984).
In the beginning of the twentieth century, Wilson (1912) introduced the term “extrapyramidal” motor system in his description of a disorder involving degeneration of the striatum (hepato-lenticular degeneration) which is known today as Wilson’s disease. Marsden latter described the motor functions of the basal ganglia based in large part on the symptoms of Parkinson’s disease (Marsden, 1980, Marsden, 1982). A debate then ensued over whether the ‘traditional’ view (notwithstanding pre-twentieth century claims) of the basal ganglia as a motor structure was exclusively supported by clinical and experimental evidence or whether empirical data also supported other nontraditional hypotheses (Cools et al., 1981, Marsden, 1981, Öberg and Divac, 1981). For example, Öberg and Divac (1979) proposed “remaining cognitive functions” of the basal ganglia that involve associative, mnemonic and complex perceptual processes. In the clinical/experimental literature, acknowledgments of “cognitive impairments” associated with neurodegenerative disorders of the basal ganglia have since become more prevalent and acceptable (e.g., Brown et al., 1997, Carlesimo et al., 1991, Cools et al., 1984, Furtado and Mazurek, 1996, Girotti et al., 1991, Levin et al., 1989, Morris et al., 1988, Owen et al., 1992, Phillips and Carr, 1987, Saint-Cyr et al., 1988). Öberg and Divac (1979, p. 307) state that “...cognition often finds expression in behavior...and the exact borderline between cognitive and motor mechanisms is not always obvious...it does not seem very surprising that inactivation or dysfunctioning of an intermediate processing station such as the [neostriatum] can give rise to both cognitive deficits and complex motor disturbances as a result of disconnection and/or aberrant information flow.”
To the extent that cognitive functions are mediated by the cerebral cortex, some component(s) of the expression of such functions are likely to, at least in part, rely on basal ganglia circuitry. Consistent with this view, several contemporary formulations of basal ganglia function have essentially merged sensory/cognitive and motor/inhibitory processes (see Table 1). For example, some of the more recently proposed functions include motor planning, mediation of motor equivalence, adaptive motor control, motor learning, control of intentional actions and voluntary movement, chunking of action repertoires, error correction in responding, strategy selection, switching aptitude, movement initiation, modulation of neural arousal, programming behavior patterns, egocentric spatial orientation, habit formation, reference memory, procedural learning/memory, response set, attention to action, attentional set-shifting, inhibition of competing motor programs, and rule potentiation. Although this is not a comprehensive list of basal ganglia theories it does serve to illustrate the diversity and scope of modern day hypotheses.
We propose that the above hypotheses may be grouped into two general categories. The first category includes those that stress the importance of the basal ganglia, or the dorsal striatum in particular, for establishing or strengthening specific responses to sensory cues as a function of the reinforcement contingencies operating in a given situation (i.e., an incremental, repetitive or recursive function). The second category includes theories that propose that the primary function of the basal ganglia is to select different behavioral responses in the presence of changing task requirements (an adaptive, flexible or cognitive function). The former category may include habit formation, procedural learning, reference memory, egocentric orientation, and rule-based learning, whereas the latter category may include motor planning, mediation of motor equivalence, adaptive motor control, control of intentional actions and voluntary movements, error correction in responding, strategy selection, switching aptitude, attentional set-shifting, response set and attention to action. The two categories are not necessarily mutually exclusive and many proposals contain the basic elements of each alternative. The categories will be referred to here as “habit formation” and “cognitive control” because these terms may be more inclusive than others within a particular group and can be expressed in simple associative conditioning terms. For the purposes of the present review, Habit formation (see below) refers to the incremental strengthening of stimulus–response (S–R) associations as a function of reinforcement (Hull, 1943, Thorndike, 1911). Cognitive control refers to the association of a stimulus–stimulus (S–S) relationship (e.g., Pavlov, 1927/1960; Tolman, 1932, Tolman, 1948) with a particular response [i.e., (S–S)–R].
The concept of habit formation has a long history in animal psychology, dating back to the positive “law of effect” proposed by Thorndike, 1911, Thorndike, 1933. In its simple form, habit formation refers to the incremental strengthening of a stimulus–response (S–R) bond according to the reinforcement contingencies operating within a given learning situation. Although the terms habit formation and S–R learning are often used interchangeably they are not necessarily the same. Habit formation focuses on the “strength” of the S–R bond which varies cumulatively across pairings. In contrast, S–R learning only identifies what is being associated but does not necessarily imply that the strength of association will change over time as a function of reinforcement. Indeed, the S–R theorist Guthrie (1942, p. 30) believed that: “a stimulus pattern gains its full associative strength on the occasion of its first pairing with a response.” Guthrie’s “all or none” theory of S–R learning is different from what is generally assumed to be the case in many contemporary discussions and in more recent theoretical models of habit formation (e.g., Hull, 1943, Hull, 1952, Rescorla and Wagner, 1972, Spence, 1936, Spence, 1956, Wagner and Rescorla, 1972).
The following review will attempt to integrate some recent neuroanatomical and neurobehavioral findings pertaining to basal ganglia function. We propose that much of the literature supports the idea that distinct striatal subregions mediate different associative processes in accord with the two basic categories of functional proposals described above. This review will conclude with a discussion of current challenges and controversies in the literature concerning these distinct striatal subregions and their functional contributions to mammalian behavior.
Section snippets
Nomenclature
The term basal ganglia refers to a group of subcortical nuclei that invariably includes the globus pallidus, substantia nigra pars reticulata, caudate nucleus and putamen (Wise, 1991). In addition, a ventral extension of the basal ganglia is now recognized to include the nucleus accumbens and olfactory tubercle. The caudate nucleus, putamen, nucleus accumbens and olfactory tubercle are collectively referred to as the striatum. The striatum receives most of the input to the basal ganglia. The
Neurophysiology of the dorsal striatum
Neurons in the striatum display sensory evoked responses when a visual, auditory or tactile stimulus is linked with a conditioned movement (Aosaki et al., 1995, Aosaki et al., 1994, Kimura, 1986, Kimura, 1995, Kimura et al., 1992, Kimura et al., 1993, Lidsky and Schneider, 1994, Rolls, 1992, Rolls, 1994, Romo et al., 1992, Schultz, 1995, Schultz and Romo, 1992, White and Rebec, 1993). The activity of striatal neurons is sometimes related to the sensory stimulus, the movement, to both events or
Behavioral-anatomical Integration
The following discussion reviews some of the findings supporting the proposed S–R habit formation and cognitive control functions of the striatum. There are two main points suggested by these findings. First, each function may be localized within different regions of the DS. Second, the function of a particular region may be related to its cortical afferents. Based on the anatomical findings indicating that the striatum is organized into parallel, partially segregated circuits, a functional
Challenges and controversies
In the remaining sections of this paper we will discuss what we see as challenges and controversies in the literature concerning the distinct striatal subregions described above and their functional contributions to mammalian behavior. First, specific definitions of the functions of the lateral and medial subregions will be presented based on an analysis of recent empirical findings. Second, several questions will be posed that if answered empirically, we believe, will broaden understanding of
Conceptual framework
Our current view is that the DS of the rat may be divided into functionally heterogeneous lateral and medial subregions (Fig. 1). The DLS, by virtue of its connections with sensorimotor neocortex, may mediate S–R habit formation with discrete modality-specific stimuli. In contrast, the DMS by virtue of its connections with allo- and mesocortical structures may mediate cognitive-spatial functions. In particular, comparison to a hippocampal-based cognitive learning and memory system will be a
Behavioral flexibility
The DMS in the rat is thought to play a critical role in behavioral flexibility (Devan and White, 1999, Devan et al., 1999, Ragozzino, Jih, et al., 2002, Ragozzino, Ragozzino, et al., 2002). Evidence for this idea comes from experiments (Ragozzino, Ragozzino, et al. (2002) in which rats are trained on a discrimination task utilizing one dimension (response or visual cue reinforced) and then the trained subjects are shifted to the other dimension. Some of these subjects received reversible
Attentional processes
An alternative view of DMS function is that it is important for egocentric space attentional processes (Christakou, Robbins, & Everitt, 2005). Support for this view was reported in a study in which the DMS was disconnected from the medial prefrontal cortex. The results showed that these subjects had a long-lasting contralesional neglect syndrome and this effect was interpreted as evidence that the DMS is part of a functional circuit that includes the medial prefrontal cortex, involved in
Instrumental learning
Some believe that the DMS is part of a neural circuit supporting a type of instrumental learning which is thought to support the early stages of goal-directed actions like bar pressing for food (Adams & Dickinson, 1981). Evidence for this functional view of the DMS comes from various approaches. One series of experiments used a two-lever discrimination task for different outcomes (Yin et al., 2005). Briefly, the role of the dorso-medial striatum in goal-directed action by assessing pre- versus
Conclusion
Just as the alternative accounts of motor and cognitive functions of the basal ganglia debated throughout the years proved to be of value in describing the complex circuitry, we propose a similar integration of contemporary hypotheses to account for the associative functions of the dorsal striatum. A wealth of accumulating evidence consistently implicates the dorsolateral striatum in S–R habit formation and the dorsomedial striatum in the cognitive control of behavioral flexibility. The next
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2020, Neurobiology of Learning and MemoryCitation Excerpt :As trial accuracy hovered at chance levels across all groups early in training (e.g., trial block 1; Fig. 1A), it appears that lidocaine treatment did not predispose rats to a turning bias or appreciably influence other non-mnemonic aspects of training. Note that the injection sites were directed at the dorsolateral striatum, a region believed to play a key role in egocentric navigation, stimulus-response learning, and habit formation (Devan, Hong, & McDonald, 2011; Packard, 1999; Packard & McGaugh, 1996; Restle, 1957; White et al., 2013; for review of striatal subregion contributions to learning and memory, see Devan et al., 2011). While our results likely reflect selective inactivation with lidocaine of the dorsolateral striatum, drug diffusion may extend beyond this subregion; thus, here we use a more conservative perspective and refer to treatment effects due to striatum as opposed to dorsolateral striatum inactivation.