Covert Representation of Second-Next Movement in the Pre-Supplementary Motor Area of Monkeys

Abstract

We attempted to analyze the nature of premovement activity of neurons in medial motor areas [supplementary motor area (SMA) and pre-SMA] from a perspective of coding multiple movements. Monkeys were trained to perform a series of two movements with an intervening delay: supination or pronation with either forearm. Movements were initially instructed with visual signals but had to be remembered thereafter. Although a well-known type of premovement activity representing the forthcoming movements was found in the two areas, we found an unexpected type of activity that represented a second-next movement before initiating the first of the two movements. Typically in the pre-SMA, such activity selective for the second-next movement peaked before the initiation of the first movement, decayed thereafter, and remained low in magnitude while initiating the second movement. This type of activity may tentatively hold information for the second movement while initiating the first. That information may be fed into another group of neurons that themselves build a preparatory activity required to plan the second movements. Alternatively, the activity could serve as a signal to inhibit a premature exertion of the motor command for the second movement.

Rank Signals in Four Areas of Macaque Frontal Cortex During Selection of Actions and Objects in Serial Order

“…It is interesting to note that the majority of studies comparing rank selectivity in the pre-SMA and SMA in the context of an arm-movement task found that the number of rank-selective neurons is higher in pre-SMA than in the SMA (Clower and Alexander 1998;Nakajima et al 2009;Shima and Tanji 2000;Sohn and Lee 2007). Our results reveal a similar trend although the difference did not achieve significance.…”

“…Although we cannot directly compare the frequencies of neurons preferring each rank to the previous studies because of the differences in the criteria for establishing preferred rank, it appears that a similar trend was observed in an oculomotor sequence task (Isoda and Tanji 2004) but not in tasks involving arm movements, in which the majority of the rank-selective neurons was preferentially active either at the beginning of the sequence (Nakajima et al 2009;Shima and Tanji 2000;Sohn and Lee 2007) or at its beginning and end (Clower and Alexander 1998).…”

“…In accordance with this view, it has been suggested that the pre-SMA is critically involved in retrieving visuomotor associations and in the initiation of sequences and sequence chunks (Kennerley et al 2004;Muri et al 1994). The latter notion has found recent support in a report by Nakajima et al (2009) showing that the activity of many pre-SMA neurons anticipates the nature of the second movement in a sequence even before the first movement has begun.…”

“…One sign of frontal-lobe involvement is the observation that numerous frontal areas contain rankselective neurons: neurons the activity of which depends on the stage the monkey has attained in a learned sequence of actions (Akkal et al 2002;Averbeck et al 2002Averbeck et al , 2003Clower and Alexander 1998;Funahashi et al 1997;Inoue and Mikami 2006;Tanji 2002, 2003;Lee and Quessy 2003;Lu et al 2002;Nakajima et al 2009;Shima and Tanji 2000;Sohn and Lee 2007). Presumably these areas act in concert to mediate serial order behavior with each making a distinctive contribution.…”

“…This issue remains unresolved because for the most part, studies of rank selectivity in different areas have been carried out under different conditions. Rank selective neurons have been observed in the frontal and supplementary eye fields (FEF and SEF, respectively) in the context of oculomotor sequence tasks Tanji 2002, 2003;Lu et al 2002), in the presupplementary and supplementary motor areas (pre-SMA and SMA, respectively) in the context of manual sequence tasks (Clower and Alexander 1998;Lee and Quessy 2003;Nakajima et al 2009;Shima and Tanji 2000;Sohn and Lee 2007; but see also Isoda and Tanji 2004), and in the dorsolateral prefrontal cortex (dlPFC) in the context of sequential tasks requiring button presses (Barone and Joseph 1989), tracing of geometrical shapes (Averbeck et al 2002(Averbeck et al , 2003, saccades (Averbeck et al 2006), and memorization of the order of presentation of a sequence of images (Inoue and Mikami 2006;Ninokura et al 2003Ninokura et al , 2004. In only a few cases were two closely related areas directly compared in the same behavioral context (pre-SMA and SMA: Clower and Alexander 1998;Nakajima et al 2009;Shima and Tanji 2000;Sohn and Lee 2007;SEF and FEF: Isoda and Tanji 2003).…”