Implementation of action sequences by a neostriatal site: a lesion mapping study of grooming syntax

Abstract

The neostriatum and its connections control the sequential organization of action ("action syntax") as well as simpler aspects of movement. This study focused on sequential organization of rodent grooming. Grooming syntax provides an opportunity to study how neural systems coordinate natural patterns of serial order. The most stereotyped of these grooming patterns, a "syntactic chain," has a particularly stereotyped order that recurs thousands of times more often than could occur by chance. The purpose of the present study was to identify the crucial site within the striatopallidal system where lesions disrupt the syntax or serial order of syntactic grooming chains without disrupting constituent movements. Small excitotoxin lesions were made using quinolinic acid at bilateral sites within the dorsolateral, dorsomedial, ventrolateral, or ventromedial neostriatum, or in the ventral pallidum or globus pallidus of rats. An objective technique for mapping functional lesions was used to quantify cell death and to map precisely those lesions that disrupted grooming syntax. Our results identified a single site within the anterior dorsolateral neostriatum, slightly more than a cubic millimeter in size (1.3 x 1.0 x 1.0 mm), as crucial to grooming syntax. Damage to this site did not disrupt the ability to emit grooming actions. By contrast, damage to sites in the ventral pallidum and globus pallidus impaired grooming actions but left the sequential organization of grooming syntax intact. Neural circuits within this crucial "action syntax site" seem to implement sequential patterns of behavior as a specific function.

Fig. 1.

Choreographed “syntactic chain” sequence of grooming actions. A choreographic transcription of a prototypical syntactic grooming chain shows the moment-by-moment trajectories of forelimb strokes over the face and the occurrence of other grooming actions. Drawings (bottom) display the actions that typify each phase of syntactic chains. To read the choreographic transcription, time proceeds from left to right. Thehorizontal axis represents the position of the rat’s nose, and stroke trajectories over the face are depicted relative to the nose. Deviations of the lines above (right paw) and below (left paw) the horizontal axis represent the elevation (level of the eye, the ear, etc.) reached by each forepaw during a stroke. Small rectangles denote paw licks. Large rectangle denotes body licking (adapted from Aldridge et al., 1990).

Fig. 2.

Map of fraction assignment within the striatopallidal system used for this study. Neuronal densities were calculated separately from core samples for each fraction. Baseline neuronal densities ranged from 12 neurons for fractions in the globus pallidus to >150 neurons in the ventrolateral neostriatum per 250 × 250 × 30 μm core sample (Table 1). For any given numbered fraction, however, neuronal density varied across different control rats by <25%.

Fig. 3.

Sequential organization after excitotoxin lesions: rates of syntactic chain completion. The percentage of first, second, third, and fourth grooming chains begun within a session that were completed syntactically (i.e., Phases I, II, III, and IV without interruption). Only rats with lesions of the anterior dorsolateral neostriatum had a reliable disruption of grooming syntax throughout a session. Abbreviations: VM STR., ventromedial neostriatum;VP, ventral pallidum; GP, globus pallidus;DM STR., dorsomedial neostriatum; VL STR., ventrolateral neostriatum; DL STR., anterior dorsolateral neostriatum.

Fig. 4.

Number of grooming actions emitted by each group. Actions emitted both within and outside of syntactic chains are included in this analysis. Rats with lesions of the ventral pallidal region had a significant decrease in the number of grooming actions. Abbreviations: Con, control; others as in Figure 3.

Fig. 5.

Examples of notated chains in control animals (right) and rats with lesions of the dorsolateral neostriatum (left). The position of the paws in relation to the face during each stroke is indicated by stroke-amplitude marker near the third chain for each group. Time (in seconds) is shown at thebottom. Choreographic notation symbols as in Figure 1.

Fig. 6.

Crucial syntax site and photomicrographs of lesions within the dorsolateral neostriatum. Photomicrographs show (A) low magnification (10×) of the anterior dorsolateral neostriatum of a vehicle-injected control rat (arrow points to location of vehicle microinjection; cc denotes corpus callosum). B, High magnification (40×) of the same anterior dorsolateral neostriatal region in vehicle-injected control rat. Note lack of neuronal death. C, Low magnification of anterior dorsolateral neostriatum in rat that received an excitotoxin lesion and had impaired grooming syntax. (Arrow points to center of excitotoxin lesion; cc denotes corpus callosum).D, High magnification of dorsolateral neostriatum after an excitotoxin lesion that impaired grooming syntax. Note paucity of neurons compared with those in B. Scale bars: Aand C, 140 μm; B and D, 40 μm.E, Map of the crucial “grooming syntax site.” Atlas view shows boundaries of the site, identified by the modified fractionator procedure, in which loss of >50% of neurons is associated with specific deficits in the sequential organization of syntactic grooming chains.