Inhibitory motor control in stop paradigms: review and reinterpretation of neural mechanisms
Introduction
Inhibition of motor responses is a concealed operation. It becomes manifest only through the absence of expected behavior. Therefore, some widely applicable methods and dependent variables from experimental psychology are inapplicable for inhibition research. This problem applies to performance (e.g., the absence of a reaction time) as well as psychophysiological reflections of inhibition (e.g., uncertainty about the moment of inhibition as a marker). We believe that this problem has led to paradoxical answers to the question where responses are inhibited, and that this is partly due to indistinctness about the exact question. In the literature, different meanings of the concept ‘locus of inhibition’ are intermingled, thus giving rise to confusion about the agent, site, and manifestation of inhibition. This paper critically reviews data that have been put forward in support of loci in subcortical, cortical, and peripheral areas of the nervous system.
Inhibition needs to be investigated through a comparison between conditions with and without response execution. It can be investigated in a laboratory setting with the stop-signal paradigm and the go/no-go paradigm. Although there may be other paradigms that probe the same inhibitory mechanisms, we only discuss inhibition of the type that is required on these two paradigms (see Logan, 1994, for a comparison between types of inhibition). On a typical stop-signal task, a subset of trials from a series of regular choice reaction time (RT) trials is interrupted by a stop signal (Logan & Cowan, 1984). The stop signal instructs the subject to withhold the response that was in preparation if possible. It becomes harder to suppress a response as the stop signal is presented closer to the moment of responding. A profile of inhibitory efficiency over time is derived by manipulating the stimulus onset asynchrony (SOA) between the response and stop signal. The stop-signal paradigm can thus be regarded as an elaboration of the go/no-go task, because in the go/no-go task, the SOA is always zero. The stimulus configuration often combines inhibition and response signals, so that the instruction can be, for example, to respond to a character (go), but not to respond when the character is presented in red (no-go).
Several authors have suggested that, in order to be successful, inhibitory processes have to win a race against concurrent response processes Lappin & Eriksen, 1966, Logan, 1981, Ollman, 1973, Osman et al., 1986, Vince, 1948. If inhibitory processes finish before the response processes do, the response is correctly withheld; otherwise, the response is executed. The formal version of the ‘horse-race model’ (Logan & Cowan, 1984) gives a rather powerful description of inhibitory control, because it is able to account mathematically for performance in the stop-signal paradigm and allows the calculation of inhibitory speed. It assumes that response processes proceed independent of stop processes.
For the calculation of stop speed, it is only necessary to know the latencies of starting and finishing the stop processes. The difference between these two latencies is known as the stop-signal reaction time (SSRT). The SOA defines the start of the stop processes, and the finish needs to be derived from other results. Given the independence assumption, the distribution of RTs on trials without a stop signal (nonsignal trials) can be used as an approximation of the covert distribution of signal RTs. The latter distribution is not entirely available because it is trimmed on the right-hand side by inhibition. It is known how much of the distribution is trimmed, because this part equals the proportion of inhibition trials. Consequently, the boundary that distinguishes between inhibition on the right and execution on the left side of the nonsignal RT distribution can be interpreted as the average finish of the stop processes (see Logan, 1994, for details).
The SSRT, which can be conceived of as an index of inhibitory efficiency, does not vary much with the primary task. It varies between 200 and 250 ms for normal adults (see Logan, 1994, for a review), and is somewhat prolonged for children (Ridderinkhof, Band & Logan, 1999) and older adults (Kramer, Humphrey, Larish & Logan, 1994). In addition, there have been reports of group differences in SSRT related to impulsivity in normal subjects (Logan, Schachar & Tannock, 1997) and children with attention deficit hyperactivity disorder (ADHD; Schachar & Logan, 1990).
Variations of the stop-signal paradigm have addressed complications of the stop processes, and the effect of the primary task onto stop processes. For this review, an interesting complication of stop processes is the requirement to stop a response, while executing an alternative response (cf. Logan & Burkell, 1986). In this stop-change condition, the inhibition latency is found to be longer than in the stop-all condition – the condition that is created by a regular stop instruction (e.g., Band, 1997). This difference in speed could simply reflect the refinement of the requirement to stop. It has been suggested, however, that there may be two separate mechanisms for stop-all and stop-change conditions (e.g., De Jong, Coles & Logan, 1995).
Logan and Burkell (1986) performed an experiment with a two-and four-choice primary task. In two stop-selective conditions, the stop signal applied only to one response, and not to the one or three other responses. SSRT was longer for selective stopping in the four-choice than in the two-choice task, and this was not the case in the stop-all conditions. Logan et al. (1997) suggested that there is a global mode for nonselective and a local mode for selective inhibition. De Jong et al. (1995), however, concluded that inhibition on a stop-selective condition requires the same mechanism as stop-all inhibition. Note that the suggestion of two modes does not imply separate mechanisms. Both for the stop-change and the stop-selective condition, it can be argued that the duration of stopping increases with the refinement of control, following a stop-signal equivalent of Hick’s law (Logan, 1994).
Some studies have looked at effects of primary-task factors onto SSRT (Kramer et al., 1994, Ridderinkhof et al., 1999. These effects are always relatively small and can be interpreted in one of two ways. They can reflect modulation of the inhibitory function (see Ridderinkhof et al., 1999, for a more extensive discussion), or they can reflect effects onto primary-task processes after the finish of the race, which lead to an overestimation of SSRT.
A hypothetical finish line, usually referred to as the point of no return (Bartlett, 1958), separates controllable from ballistic response-related processes. The duration of ballistic processes may be under experimental control, and has no effect on the chance of response inhibition. If ballistic processes contribute to RT, the actual latency of the stop processes is shorter than the race model estimates it to be.
Several studies have investigated the extent of ballistic processes in order to localize inhibitory effects (see Logan, 1994). Factors that seemed to affect processes before the locus of inhibition include stimulus discriminability Logan, 1981, Osman et al., 1986, stimulus-response compatibility (Logan, 1981), and response complexity (Osman, Kornblum & Meyer, 1990). In contrast, repetition vs. nonrepetition of stimulus-response pairs seemed to affect processes after the point of no return (Osman et al., 1986). Although this combination of results does not allow a precise localization of the point of no return, there is consensus that the contribution of a ballistic component to primary task RT cannot be large (see Logan, 1994). In other words, there is a locus of response inhibition close to execution.
The existence of a late locus of inhibition does not imply that inhibition is always exerted at that same moment. If the success of response inhibition depends only on the relative finishing time of the inhibitory and response processes, there may be multiple sites of inhibition, although the source may be the same. The point of no return represents only the last possible site of inhibition.
Section snippets
The executive-control model
Logan and Cowan (1984) proposed a model for the architecture of response inhibition and other forms of executive control. The high similarity of SSRT measurements across stop-all conditions was interpreted as support for a universal mechanism for the inhibition of a variety of response processes (e.g., Logan, 1994). Logan and Cowan’s model of executive control includes an executive that orchestrates lower-level subsidiary processes that perform the actual operations. The executive-control
Neurophysiology of response activation
Response-generating processes pass through a number of consecutive processing phases – whether in strict sequence or more in parallel. Fig. 1 shows a simplification of the architecture that underlies the initiation of responses. Two loops lead along cortical as well as subcortical motor structures, and these loops operate sequentially (cf. Goldberg, 1985). In the first (medial) loop, virtually all regions of the cerebral cortex project via the basal ganglia and motor nuclei of the thalamus
Overview
The distinction between response inhibition operating upstream or downstream from the motor cortex has had a substantial influence on the discussion about response inhibition and about the interpretation of psychophysiological data. We feel, however, that the conclusions that have been drawn from data of De Jong et al. (1990, 1995) and Jennings et al. (1992) were premature. It will be shown that the same data can be interpreted with a single inhibitory mechanism in the frontal cortex, possibly
Data supporting subcortical agents of inhibition
There is a large body of data that support forebrain and frontal cortex involvement in inhibition. It was shown in Fig. 1 which neural structures take part in the preparation of a response. The same order of structures will now be followed to discuss possible loci of inhibition. Recall that there are two looping paths between the cortex and subcortical structures. One leads along the cerebellum, one leads along the basal ganglia, and both pass relay nuclei in the thalamus. The cerebellum does
Acknowledgements
This research has been made possible with the help of the Netherlands Organization of Scientific Research (NWO/SGW grants 575-63-082 and 575-25-004). We thank Cees Brunia, the editor Maurits van der Molen, Richard Ridderinkhof and two anonymous reviewers for valuable comments on earlier versions of the paper
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