NEURONAL CODING OF SERIAL ORDER: Syntax of Grooming in the Neostriatum

How does the brain create rule-governed sequences of behavior? An answer to this question may come from a surprising source: the neostriatum (caudate nucleus and plltamen). Traditionally, the neostriatum has been considered part ofthe brain's motor system, but its colltribution to the preparation or execution of movement is recognized generally to concern high-level motor functions. Recent work implicates the neostriatum in disorders of sequential action and thought, as in the repetition of thoughts or habits in human obsessive-compulsive disorder and movements or speech in Tourette's syndrome. Yet there is no direct evidence to support the idea that the neostriatum controls sequences of behavior. Using ethological and neurophysiological techniques to study neural activity in the rat neostria111m during syntactic grooming sequences, wefound that neuronal activity in the anterolateral neostriatum depended on the execution ofsyntactic sequences of grooming actions. The individual grooming movemellts themselves did not activate the neostriatum; activation was determined by the syntactic sequence in which grooming movemellts were performed. These data provide the first direct evidence that the neostriatum coordinates the control ofrule-governed behavioral sequences. A child's first spoken sentence, the tying of one's shoelace, and the opening of a nut by a squirrel all share something in common. Each of these tasks requires the activation of a set of skilled behavioral elements. In order to be effective, each element must be activated at the proper time and in the proper serial order: These tasks are sequential. In so many tasks in human and animal life, it is Address correspondence to J. Wayne Aldridge, University of Michigan, Neuroscience Bldg., 1103 East Huron St., Ann Arbor, MI 48104-1687. not enough to know what to do: One must also know when and in which order to do it. Nearly every action, word, and thought produced by a brain relies on its serial relation to other actions, words, and thoughts for part of its significance. Even movements must be arranged serially according to rules of "action syntax" in order to form meaningful acts, just as words must be arranged syntactically to form meaningful sentences (Lashley, 1951). Patterns of serial order in behavior are old and phylogenetically pervasive. Early in the evolution of the brain, natural selection must have produced a solution in the form of neural systems to generate rule-governed sequences of behavior. These neural systems might first have evolved to sequence simple patterns of behavior, such as particular sequences of grooming, feeding, and social actions, and later have been extended to control the serial order of human language and thought. We have capitalized on the primacy of simple behavioral sequences in mammalian evolution by using simple sequences to reveal brain systems that control the serial pattern of behavior. Our strategy has been to study the role of neural circuits within the neostriatum. Recent work indicates that the neostriatum participates in high-level aspects of motor control (Aldridge, Anderson, & Murphy, 1980a; Alexander & Crutcher, 1990; Jaeger, Gilman, & Aldridge, 1993; . Marsden, 1982, 1984; Oberg & Divac, 1979). In addition, there is mounting evidence that neostriatal circuits are uniquely crucial to the serial coordination of some behavioral sequences (Berridge & Whishaw, 1992). Two types ofevidence are required to assert that a neural system controls the serial order of behavioral sequences. First, lesions of the neural system should disrupt the sequential organization of a behavior event but spare the behavioral elements. Second, neurons within the neural system must show activation patterns that are correlated specifically with the sequence of such behavioral patterns rather than with their elemental constituents. Regarding the first type of evidence for the neostriatum, it is becoming clear that a variety of human disorders, such as Parkinson's, Huntington's, and Tourette's syndromes, can produce special deficits in the sequential organization of movement and language (Agostino, Berardelli, Formica, Accornero, & Manfredi, 1992; Benecke, Rothwell, Dick, Day, & Marsden, 1987; Frankel et aI., 1986; Harrington & Haaland, 1991; Lieberman et aI., 1992; Stelmach, Worringham, & Strand, 1987; Trimble, 1989). But human neurological disease disrupts many aspects of behavior besides sequential organization. More precise correlations between serial order and neural systems can be obtained by studies of animal behavior. The neostriatum is crucial for the sequential pattern of rule-governed chains of rodent grooming behavior (Berridge & Fentress, 1988; Berridge & Whishaw, 1992; Cromwell & Berridge, 1990). For example, in one grooming sequence, up to 25 forelimb and body movements are linked in a "syntactic" chain that comprises four sequential phases. This syntactic chain of grooming actions occurs with a probability that is vastly higher than would be expected by a chance combination of the individual movements (Fig. I). Conveniently for the analysis of whether brain systems contribute to the sequence or the individual movements of this syntactic grooming chain, the same movements that make up the syntactic chain occur frequently in other nonchain sequences that do not exhibit a rigid syntax. Providing the first type of evidence for sequential control, damage to the anterolateral neostriatum disrupts the integrity of syntactic grooming chains, but does not disrupt the occurrence of constituent grooming movements outside the chain (Berridge & Fentress, 1988; Cromwell & Berridge, 1990). This conVOL. 4, NO.6, NOVEMBER 1993 Copyright © 1993 American Psychological Society 391 at UNIV OF MICHIGAN on December 8, 2015 pss.sagepub.com Downloaded from PSYCHOLOGICAL SCIENCE Neuronal Coding of Sequence CHAIN GROOMING 400 g) were anesthetized with ketaminexylazine and implanted with a permanent, vertically movable electrode in the rostral lateral neostriatum. The electrode was designed for painless extracellular recording from multiple individual neurons during free spontaneous behavior (Aldridge, Berridge, & Herman, 1990). An amplifier mounted near the electrode was connected to the recording computer by a commutator that permitted free movement in a circular recording chamber. The electrode implant did not cause discomfort and did not interfere with normal behavior in the rat's home cage. The entire behavioral testing procedure was free of distress for the rats. Beginning a week after implantation, behavior was videotaped and neuronal discharge activity was recorded for I or more hours while the animals groomed and moved about freely. A frame-byframe analysis of the videotaped grooming sequences was conducted subsequently (Berridge, 1990; Berridge & Fentress, 1986) to find the onset and offset times of movements. Twenty-three different behavioral events were evaluated, including the component movements of syntactic chain grooming (Phase I = synchronous rapid strokes by both paws over the nose; Phase II = strokes by a single paw along the side of the face; Phase III = synchronous large strokes by both paws over the eyes or ears; Phase IV = licking of the body flank) and their nonchain equivalents, and of a visual stimulus (a I-em-square flag that moved toward the eye), and tactile stimulation (brushing and light touching) of four body regions. Each of these behavioral events occurred spontaneously, except sensory stimuli, which were presented several times per hour. Individual neurons were identified and discriminated from each other by the computer after recording on the basis of spike waveform shape. The onset and offset times of more than 6,000 behavioral events were entered into the computer and used to Construct 683 perievent time histograms for 34 neurons at 21 recording sites. Each perievent time histogram (Figs. I and 2) representing several repetitions of the same behavioral event was analyzed quantitatively (Macpherson & Aldridge, 1979). Most neurons (94%, 32/34) re-sponded to at least one of the 23 behavo BODY LICKING