Coding of serial order by neostriatal neurons: a "natural action" approach to movement sequence

Abstract

The neostriatum controls behavioral sequencing, or action syntax, as well as simpler aspects of movement. Yet the precise nature of the neostriatums role in sequencing remains unclear. Here we used a "natural action" approach that combined electrophysiological and neuroethological techniques. We identified neostriatal neurons that code the serial order of natural movement sequences of rats. During grooming behavior, rats emit complex but highly predictable species-specific sequences of movements, termed "syntactic chains." Neuronal activity of 41% of cells in the dorsolateral and ventromedial neostriatum coded the sequential pattern of syntactic chains. Only 14% coded simple motor properties of grooming movements. Neurons fired preferentially during syntactic chains compared with similar grooming movements made in different sequential order or to behavioral resting. Sequential coding differed between the dorsolateral and ventromedial neostriatum. Neurons in the dorsolateral site increased firing by 116% during syntactic chains, compared with only a 30% increase by neurons in the ventromedial site, and dorsolateral neurons showed strongest coding of grooming syntax by several additional criteria. These data demonstrate that neostriatal neurons code abstract properties of serial order for natural movement and support the hypothesis that the dorsolateral neostriatum plays a special role in implementing action syntax.

Fig. 1.

Recording sites in neostriatum. Each recorded cell is indicated as responsive to syntactic chains of grooming movements (circle), nonresponsive to any grooming movement (Y symbol) or responsive only to grooming movements occurring outside of syntactic chains (nonchain,triangle). Electrode recording sites from planes 0.5 to −0.1 referenced to bregma (Swanson, 1992) were plotted onto sections 0.45 or 0.00 (within 0.2 mm) and dithered (for illustration) within a 0.25 mm radius around the lesion site. Because responsive and nonresponsive cells were recorded simultaneously, their anatomical locations were often adjacent, and so symbols overlap extensively.

Fig. 2.

Coding of behavioral state by neurons in dorsolateral (top) and ventromedial (bottom) neostriatum. Median firing rates during syntactic grooming chains (C), nonchain grooming (N), and behavioral rest (R) are shown by the vertical box plots in the insets at left(median rates were determined separately for each neuron). Thedifferences between rates for each pair of behavioral states compared (Chain vs Rest,Nonchain vs Rest, andChain vs Nonchain) are illustrated by thehorizontal box plots. Dashed vertical line at zero indicates no difference in the two states being compared. Each box encompasses the central 50% of the sample (25th–75th percentiles), the median value is indicated by themiddle line in each box, and the whiskers extend 1.5 times the distance between the border of the box and the median value of the quadrant. Dorsolateral neurons differed significantly in absolute median firing rates (vertical bars, inset graph) across groups (Friedman two-way ANOVA,p < 0.001). The within-neuron behavioral state comparisons (horizontal boxes) revealed a significant shift from zero toward positive values (one-sample ttest, H₀ = 0; Bonferroni adjustedp = < 0.01; designated by *). By contrast, ventromedial neurons did not differ significantly in either absolute median firing rates (inset graph, Friedman two-way ANOVA, p = 0.2) or in direct comparisons of the various behavioral states (horizontal boxes, one-samplet test, H₀ = 0; Bonferroni adjusted p = > 0.05).

Fig. 3.

Neuronal coding of syntactic grooming phases. The schematic drawings (A–D) show the four phases of syntactic grooming chains in the order they appear. A choreography diagram (top) illustrates the movement trajectory of the forelimbs as a function of time and distance from the midline (vertical dimension). The inset diagram to the leftof the choreography diagram shows a rat’s face as viewed from below on the video monitor on which the distances were determined. The excursions from the midline are measured from the midline to the center of the hand (Y dimension on this drawing) with the base of the vibrissae, eyes, and ears as landmarks. The bottom row of perievent time histograms and rasters from four different neurons illustrates neuronal activity changes of neurons that responded to a particular phase. Each example is a separate neuron in the dorsolateral striatum except C, which was recorded from ventromedial striatum. All four have increases in activity associated with the phase onset, which is at time = 0 in each histogram and raster. The histogram represents the average firing rate (y-axis) in bins 50 msec wide. The marks in each spike train of the raster indicate the time in the spike train at which the preceding or following phase began. In A, the marks indicate phase 2 onset. In B, marks indicate phases 1 (time < 0) and 3 (time > 0). In C, marks indicate phases 2 (time < 0) and 4 (time > 0; note some are >2 sec and do not appear). In D, marks indicate phase 3. The spike trains are sorted in the order of increasing phase 1 duration (A, B), phase 2 duration (C), and phase 3 duration (D). Neuronal activity generally occurs at about the same time as movement onset except for the neuron in phase 4, in which the change in activity precedes the onset of body licking.

Fig. 4.

Proportion of grooming responses by neostriatal neurons. Ventromedial neurons are represented on theleft (n = 37), and dorsolateral neurons are shown on the right (n = 79). The proportions of neurons that exhibited activity changes during chain grooming bouts are shown as the excised portions of the circles. A portion of these chain-responsive neurons also respond during nonchain grooming (cross-hatching). There are more responsive neurons in the dorsolateral striatum overall and particularly, more neurons that responded to syntactic grooming chains. The relatively small proportions of neurons responding only during nonchain grooming are indicated by open hatching. Neurons with no response to grooming behavior are marked bydotted hatching.

Fig. 5.

Sample dorsolateral neuron during entire recording session. The rate meter graph (5 sec bin) on theleft demonstrates the slow and irregular firing pattern of a single neuron in the dorsolateral neostriatum, typical of striatal neurons, recorded over ∼8000 sec (2.2 hr). During this time seven syntactic chains occurred and are indicated by trianglesunder the x-axis. A perievent histogram aligned to the onset of the same seven syntactic chains (right, displays ∼1 min periods) shows the neuron is still dominated by chain-related activity when examined in a more fine-grained analysis. The filled triangles on each raster line indicate the end of the grooming chain. The dashed linesunder each raster line indicate periods of nonchain grooming that preceded or followed the chain.

Fig. 6.

Proportion of neurons that coded particular syntactic phases of grooming chains. Left, The proportions of responsive neurons (expressed as a percentage of total neurons tested on y-axis) are shown for each phase of the syntactic chain. Dorsolateral neurons were more responsive in every phase in comparison to ventromedial neurons. Right, Multiphase versus single-phase neurons. Dorsolateral neurons were also more likely than ventromedial neurons to have responses during more than one phase of the chain. In contrast, most ventromedial neurons are more likely to have a response during only a single phase of the chain.

Fig. 7.

Phasic activity changes during grooming chains. The bars represent the average change in neuronal firing from the onset of the phase until 300 msec after the onset, expressed as a percentage of the average activity in the period from −2 to −1 sec before the chain began. SE values are indicated on each bar. A value of zero (dashed baseline) indicates no change relative to the prechain period. Values <0 indicate a relative decrease in rate. Each bar represents one phase. Phase 5 represents the time period at which body licking ended. Thegraph on the right indicates the average for all five periods. Solid bars, Dorsolateral striatum;hatched bars, ventromedial striatum.

Fig. 8.

Neostriatal coding of syntax versus movement. This neuron in the dorsolateral striatum was activated during phase 3 (Bilateral strokes) of the syntactic grooming chain (left) but was not responsive to bilateral grooming strokes that were performed outside of the chain during sequentially flexible bouts of nonchain grooming (right). In other words, the neuron did not code the kinematic or dynamic properties of the bilateral strokes but rather was sensitive to features of these movements in the context unique to syntactic chains. The actual forelimb movements are shown by the choreographed trajectory representations superimposed on each spike train (format as in Fig. 3). The onset of the bilateral stroke, which is the alignment point for these spike trains and histogram, begins at time = 0. Thevertical axis to the left of thebottom trace in the raster on the leftindicates the excursion dimensions in the same format as the one shown in Figure 3. Whereas the trajectories of nonchain grooming strokes were often smaller in amplitude, the two forepaws made similar movements over the face below the ears (in terms of stroke morphology, pattern, and time course) during syntactic chains and nonchain grooming. This particular neuron was also responsive during phase 1 of the chain, as indicated by the peak in the histogram at about −0.8 sec. Themarks above each raster line indicate the time at which the phase 1 strokes began.

Fig. 9.

Syntax versus movement comparisons for each phase. Neuronal activity recorded during chain grooming (top row) and nonchain grooming (bottom row) was compared for chain-responsive neurons. Four different dorsolateral striatal neurons are shown, with one example for each of the first four phases of chain grooming sequence. The motorically equivalent nonchain stroke for the same cell is shown below. The most common finding was the absence of a response during nonchain grooming movements (three leftmost neurons). The neuron on theright was unusual; it had an excitatory response before flank licking with no change after the phase onset. At the onset of flank licking in nonchain grooming, an inhibitory response was evoked. The marks above phase 1 raster lines indicate onset of phase 2. Marks above phase 2 rasters indicate onset of phase 1 (open circles) and onset of phase 3 (filled circles). In phase 3 raster,marks indicate onset of phase 2. The rasters with event markings have been ordered from top tobottom with decreasing time between the alignment event and the first mark on the raster line.

Fig. 10.

Timing of neuronal activity. The timing relationships of neuronal activity to the onset of movement is shown for three dorsolateral neurons. The format of each perievent histogram is similar, with the onset of the first movement in the phase aligned to time = 0 on the x-axis. In every case neuronal activation occurs at about the same time of the movement or else follows the onset of the movement. Left, A neuron activated during phase 1 of the chain (Elliptical strokes) is shown. The marks in each spike train after time = 0 indicate the onset time of phase 2.Center, Another neuron responsive to the onset of phase 3 (Bilateral stroke). The marks before the time 0 axis indicate the onset of phase 2. The marksafter time 0 (where visible) indicate the onset of phase 4.Right, A different dorsolateral neuron illustrates a similar timing relationship to a nonchain large unilateral stroke with the right limb (recording on left side of striatum).