Disrupting Short-Term Memory Maintenance in Premotor Cortex Affects Serial Dependence in Visuomotor Integration

Abstract

Human behavior is biased by past experience. For example, when intercepting a moving target, the speed of previous targets will bias responses in future trials. Neural mechanisms underlying this so-called serial dependence are still under debate. Here, we tested the hypothesis that the previous trial leaves a neural trace in brain regions associated with encoding task-relevant information in visual and/or motor regions. We reasoned that injecting noise by means of transcranial magnetic stimulation (TMS) over premotor and visual areas would degrade such memory traces and hence reduce serial dependence. To test this hypothesis, we applied bursts of TMS pulses to right visual motion processing region hV5/MT+ and to left dorsal premotor cortex (PMd) during intertrial intervals of a coincident timing task performed by twenty healthy human participants (15 female). Without TMS, participants presented a bias toward the speed of the previous trial when intercepting moving targets. TMS over PMd decreased serial dependence in comparison to the control Vertex stimulation, whereas TMS applied over hV5/MT+ did not. In addition, TMS seems to have specifically affected the memory trace that leads to serial dependence, as we found no evidence that participants' behavior worsened after applying TMS. These results provide causal evidence that an implicit short-term memory mechanism in premotor cortex keeps information from one trial to the next, and that this information is blended with current trial information so that it biases behavior in a visuomotor integration task with moving objects.SIGNIFICANCE STATEMENT Human perception and action are biased by the recent past. The origin of such serial bias is still not fully understood, but a few components seem to be fundamental for its emergence: the brain needs to keep previous trial information in short-term memory and blend it with incoming information. Here, we present evidence that a premotor area has a potential role in storing previous trial information in short-term memory in a visuomotor task and that this information is responsible for biasing ongoing behavior. These results corroborate the perspective that areas associated with processing information of a stimulus or task also participate in maintaining that information in short-term memory even when this information is no longer relevant for current behavior.

Keywords: TMS; hV5/MT+; premotor cortex; serial dependence; short-term memory; visuomotor integration.

Figure 1.

Overall procedure and TMS trial schematics. A, In three separate sessions, participants were screened for TMS and fMRI suitability (session 1), performed an fMRI localizer experiment to individually determine TMS target sites (session 2), and performed the main coincident timing task while we applied TMS at hV5/MT+, PMd, or Vertex (session 3). B, On each trial of the main task on the first and on the TMS sessions, participants were presented a target moving rightwards and were required to press a button at the same time as the target hit the interception zone. We applied TMS bursts 500 ms into the pause between trials. TMS bursts were 500 ms long.

Figure 2.

Stimulus conditions of the functional localizer tasks and illustration of TMS stimulation sites. Left PMd and right hV5/MT+ were individually defined using fMRI in a separate localizer experiment preceding the TMS experiment. A, Left PMd was defined as the region showing increased BOLD signal when intercepting moving targets (left) contrasted against only viewing moving targets (middle) and performing a reaction time task (right). B, Right hV5/MT+ was defined as the region showing increased BOLD signal when participants viewed moving dots (left) at the left visual hemifield contrasted with static moving dots (right). C, Illustration of TMS stimulation sites at right hV5/MT+, left PMd, and Vertex. Vertex was defined individually on the anatomic images.

Figure 3.

Behavioral results. A, Temporal error as a function of previous and current trial speeds for No-TMS, Vertex, right hV5/MT+, and left PMd conditions. Blue indicates positive temporal errors and red indicates negative temporal errors. B, Previous trial speed slopes of the multiple linear regressions for each participant at the No-TMS, Vertex, right hV5/MT+, and left PMd conditions. Red circles represent slopes for multiple linear regressions of each participant, black open circles represent the mean slope values across participants within each condition, and error bars represent the SD. C, Previous trial speed slope differences between PMd and hV5/MT+ against Vertex. Blue circles represent differences in slopes between conditions for each participant, black open circles represent the median differences between conditions, and error bars represent the interquartile range for differences in slopes between conditions; *p < 0.05; n.s., p > 0.05.

Figure 4.

Absence of evidence for a TMS effect on the current trial apart from serial dependence. Temporal error (ms, A) and variable error (ms, B) averaged over previous and current trial speeds on No-TMS, Vertex, right hV5/MT+, and left PMd conditions. Blue circles represent the average temporal and variable errors for each participant. Black open circles represent the mean temporal and variable errors within conditions. Error bars represent SD within condition.