A cortical mechanism linking saliency detection and motor reactivity in rhesus monkeys

Abstract

Sudden and surprising sensory events trigger neural processes that swiftly adjust behavior. To study the phylogenesis and the mechanism of this phenomenon, we trained two rhesus monkeys to keep a cursor inside a visual target by exerting force on an isometric joystick. We examined the effect of surprising auditory stimuli on exerted force, scalp electroencephalographic (EEG) activity, and local field potentials (LFP) recorded from the dorso-lateral prefrontal cortex. Auditory stimuli elicited (1) a biphasic modulation of isometric force: a transient decrease followed by a corrective tonic increase, and (2) EEG and LFP deflections dominated by two large negative-positive waves (N70 and P130). The EEG potential was maximal at the scalp vertex, in all respects similar to the human "vertex potential". Electrocortical potentials and force were tightly coupled: the P130 amplitude predicted the magnitude of the corrective force increase, particularly in the EEG electrodes contralateral to the limb exerting force, and in the LFP recorded from deep rather than superficial cortical layers, suggesting a direct effect of the vertex potential on the motor output determining the behavior. These results disclose a phylogenetically-preserved cortico-motor mechanism supporting adaptive behavior in response to salient sensory events.

Neural encoding of musical expectations in non-human primates

“…Two male rhesus monkeys (Macaca mulatta) reared without music exposure were tested: Monkey M (11 years old, 10 Kg) and Monkey T (11 years old, 9.8 Kg). The animals were previously involved in other studies 44 and trained to sit on a primate chair, with their head fixed, wearing an ad hoc tailored EEG cap (http://www.easycap.de). The animals had no restrictions on food and water, both before and after the experimental sessions.…”

“…AF3 and AF4 were not excluded because they were necessary for the automatic detection of eye-related artefacts (see below). The data were further de-noised in EEGLAB using a validated algorithm for automatic artefact-correction: Artefact Subspace Reconstruction (ASR, threshold value 5) 80 , previously applied to human and monkey EEG data 44,81 . Eye-movement artefacts were corrected using another automatic artefact-correction algorithm implemented in EEGLAB: ICLabel 82 .…”

“…Event-related potential (ERP) analyses were conducted by segmenting the EEG data into 200 ms epochs, starting 50 ms before the onset of each note, and ending 150 ms following the onset. This time window was chosen based on the observation that monkeys' ERPs (namely the P30, the N70 and the P130) exhibit earlier latencies than their human homologous (P50, N100 and P200) possibly due to anatomical differences in the length of the recruited fibre tracts 44,83 . To quantify the ERP modulation as a function of note surprise, we selected the notes associated with the highest and lowest 20% S values for each melody.…”

“…Specifically, we observed a significant cluster capturing higher EEG amplitude in response to unexpected notes (Monkey 1: p < .001, electrodes: AF3-4, F1-z-2, FC5-3-1-z-2-4, Cz; Monkey 2: p < .001, electrodes: F1-z-2, FC3-1-z-2, Cz). The time window of this modulation is reminiscent of ERP components associated with prediction error, previously characterised in monkeys 44 and humans 45 . This effect of surprise observed while listening to Real music indicates optimised detection of unexpected events within structured contexts, in line with human 46,47 and rodent studies 48 .…”