Oscillatory activity in sensorimotor cortex of awake monkeys: synchronization of local field potentials and relation to behavior

“This supports previous findings that low frequency oscillations can be used to differentiate movement from rest, but are not highly modulated with the details of movement (Chestek et al., 2013; Flint et al., 2012b; Murthy and Fetz, 1996).”

“Furthermore, interhemispheric 587 synchronization during bimanual and unimanual motor tasks was observed in 588 monkey motor cortex for activity in the beta-frequency band (Murthy and Fetz, 1996).”

“Furthermore, since significant EEG-EMG coherence was observed in the -band, as previously reported (3, 9, 12, 16, 19, 25, 27, 35, 37, 41, 48), we examined the muscle fatigue-induced changes in same frequency component of the force signal by determining the sum of the auto-PSD function of the force between 15 and 35 Hz…”

“Similar findings were also obtained for the posterior parietal cortex and frontal cortex (Vaadia et al., 1995; Murthy and Fetz, 1996a,b; Riehle et al., 1997; Lee et al., 1998; Funahashi and Inoue, 2000; Baker et al., 2001; Constantinidis et al., 2001).”

“In primates, gamma band-synchronized oscillations in the arm areas of motor and somatosensory cortex have been linked to arm movements, although they also occurred spontaneously (46, 72, 73).”

“…evidence suggests that selective attention might not need to be implemented by enhanced firing rates but could be implemented by enhanced oscillation or synchrony in neuronal ensembles, particularly in the early visual areas (Murthy & Fetz, 1996; Fries et al., 2001; Steinmetz et al., 2000).”

“1Zanvyl Krieger Mind/Brain Institute, Johns Hopkins University, Baltimore, Maryland; and 2Harrington Bioengineering, Fulton School of”

“The motor cortex exhibits resting-state synchronization of the oscillations at beta frequency band [36,37].”

“…led the authors to conclude that synchronisation of LFP oscillations appears too non-specific to be directly involved in mediating the control or execution of movements but may rather have a more general role in higher-order and attention-related aspects of motor behaviour (Murthy and Fetz 1996a).”

“In direct support of this idea, neocortical alpha/beta power decreases (a proxy for neural desynchrony; Buzsáki et al., 2012 ; Murthy and Fetz, 1996 ) have been shown to correlate with the enhanced fidelity of neural representations sources of information into a coherent memory trace ( Griffiths and…”

“…for high-frequency oscillations in individual stimulus trials because oscillations may occur momentarily and go undetected in the summed ACGs, especially if the predominant oscillatory frequency varies across trials (Ghose and Freeman, 1992; Murthy and Fetz, 1996b; Gray and Viana Di Prisco, 1997).”

“Most researchers consider that higher corticomuscular interaction comes from high attention demands towards the motor task (Jantzen et al., 2001; Kristeva-Feige et al., 2002; Murthy and Fetz, 1996).”

“Synchronization between cortical and muscle activity is most pronounced in the beta band range during steady muscle contractions as shown in monkeys (Murthy and Fetz, 1992, 1996; Sanes and Donoghue, 1993; Baker et al., 1997, 1999) and humans (Conway et al., 1995; Halliday et al., 1998; Mima and…”

“For the last ten years, research on the beta-range CMC has shown that it is task dependent [4,5], that it reflects attention and precision [6,7], compliance of the gripped objects [8,9], displacement [10], magnitude of force [11] and learning processes [12].”

“The ability of beta power to fluctuate in time has been recognized for several decades (Murthy and Fetz, 1992, 1996).”

“The dura was incised with a fine needle to expose the surface of the cortex.”

“Previous monkey studies demonstrated the occurrence of ␤-band oscillations in local field potentials and unit activity in the primary motor cortex when performing motor tasks (Donoghue et al. 1998; Murthy and Fetz 1992, 1996a,b; Sanes and Donoghue 1993 ).”

“…activity appeared during increased alertness without any regular relation to the limb movements (Bouyer et al., 1981; Sheer, 1984; Murthy and Fetz, 1996a) and that the synchronization oc- curred in both task-related and unrelated neurons in the sensorimotor cortex (Murthy and Fetz, 1996b).”

“Physiological neuronal network oscillations at beta frequency (15–35 Hz) occur spontaneously in the primary motor cortex (M1) of humans (Jensen et al., 2005; Hall et al., 2010a) and in animal models (Murthy and Fetz, 1996; Baker et al., 1997).”

“These areas have known mono- or disynaptic connections with S1BF (Paperna and Malach, 1991; Naber et al., 1999; Aronoff et al., 2010).”

“Hence, a modulatory effect of preactivated motor programs on poststimulus GBR is conceivable only for young children (Murthy & Fetz, 1992; Jokeit & Makeig, 1994; Murthy & Fetz, 1996; Roelfsema et al., 1997).”

“…activity has been interpreted as a global state reflecting task engagement (Rougeul et al., 1979; Donoghue et al., 1989) or attentional state (Murthy and Fetz, 1996) in the motor cortex and expectation (CardosodeOliveira et al., 1997;Worden et al., 2000) or attention (Fries et al., 2001) in…”

“9, A(i), top], consistent with previous observations (Madler et al., 1991; Murthy & Fetz, 1996; Okun et al., 2010; Xing et al., 2012).”

“To assess the effect of interelectrode separation on correlation magnitude within PFC and PPC, we plotted the correlation magnitude versus distance for all pairs within PFC, and together for all pairs on the same side of the IPS.”

“Withmicromanipulators (MO-8, Narishige, East Meadow, NY, USA), single barrel glass recording electrodes filled with 2% Pontamine Sky Blue dye in 2 M NaCl were lowered through craniotomies to the PPN or MCx. Spike trains and LFPs were recorded with microelectrodes with 3–4 MΩ resistances (measured at 135 Hz) with tip d…”

“Brackets indicate SE.”

“Synchronized oscillatory activity in the beta-frequency band (15–30 Hz) can be observed over the sensorimotor cortex of primates and humans (Donoghue et al., 1992, 1998; Murthy and Fetz, 1992, 1996b; Sanes and Donoghue, 1993; Baker et al., 1999).”

“Synchronization between sensory and motor assemblies has been investigated in a number of studies in cats, monkeys, and humans during execution of tasks requiring sensorimotor coordination (Murthy and Fetz 1996; Roelfsema et al. 1997; Aoki et al. 2001).”

“…circuits of the parietal cortex and motor cortices contain widespread beta-frequency band LFP activity (Donoghue et al. 1998; Kilavik et al. 2011; Murthy and Fetz 1996; Pesaran et al. 2008), suggesting that reach-related modulation of area LIP responses could originate in these circuits and…”

“In the motor areas, most studies have been devoted to explore the specificity of the different LFP’s frequency bands during planning or execution of eye/arm movements (Sanes and Donoghue, 1993; Murthy and Fetz, 1996; Donoghue et al., 1998; Buneo et al., 2003; Mehring et al., 2003; Rickert et al., 2005; Heldman et al.,…”

“behavioral task performances [16–19], which has been proposed”

“Periodic oscillations may play a functional role in behavioral arousal [24] or the increased perceptual attention involved in exploratory movements [20].”

“Indeed, premovement beta desynchronization over motor regions has been interpreted as reflecting their level of activation (Pfurtscheller and Berghold, 1989; Sanes and Donoghue, 1993; Murthy and Fetz, 1996; Schnitzler et al., 1997).”

“The manipulation of burst dynamics may be a means of selectively improving motor impairment. tions, where it takes the form of relatively short-lived phasic bursts in basal ganglia-cortical motor circuits (Murthy and Fetz, 1992, 1996; Feingold et al., 2015; Deffains et al., 2018).”

“The mu (8–12 Hz) and beta (12–30 Hz) bands also contain substantial movement-related information (Murthy and Fetz 1996; Sanes and Donoghue 1993), but this tends to be more useful in discriminating movement vs. rest (Williams et al. 2013) than in predicting directional information.”

“…frequency also coincides with the characteristic frequency of the physiological cortical gamma oscillation, which was first discovered in 1942 in the olfactory cortex (Adrian 1942) and subsequently during the 1980s and 1990s in many parts of the neocortex (Gray et al. 1989; Murthy and Fetz 1996).”

“…and probably represent a form of synchrony in the nervous system different from the coherent oscillatory synchrony at 15–40 Hz that can be demonstrated in the motor cortex and EMG (Baker et al. 1997; Conway et al. 1995; Donoghue et al. 1998; Kilner et al. 1999, 2000; Murthy and Fetz 1996b).”

“In particular, action-contingent synchronization has been observed between motor and somatosensory areas of the monkey (Murthy & Fetz, 1992, 1996), and across the visual and parietal cortex and the parietal and the motor cortex of the cat (Roelfsema, Engel, Koenig, & Singer, 1997).”

“Although LFP signals recorded in motor cortex from electrodes separated by up to several millimeters are typically highly correlated (Murthy and Fetz, 1996a), the analysis of the instantaneous phase of the oscillation (e.”

“It is also known that excitability is enhanced at particular phases of the beta oscillation (Murthy and Fetz, 1996) (See also Figure 1b,c).”

“…the sensorimotor cortex of monkeys and humans have synchronous oscillatory activity in the 15–30 Hz range (Jasper & Penfield, 1949; Gastaut, 1952; Murthy & Fetz, 1992, 1996a,b; Sanes & Donoghue, 1993; Salmelin & Hari, 1994; Stancak & Pfurtscheller, 1996; Baker et al., 1997; Donoghue et al.,…”

“Extrapolating these hypotheses to the motor system would suggest that the motor cortex oscillations could also be involved in attention to aspects of movement (Donoghue et al., 1998; Murthy and Fetz, 1996a).”

“…shown that the spectral content of LFP signals in the basal ganglia-thalamo-cortical network in rats (Leventhal et al 2012) and non-human primates (Sanes and Donoghue 1993, Murthy and Fetz 1996, Courtemanche et al 2003) is modulated during the use of a cue and the generation of voluntary movements.”

“Previous studies have shown that -LFP power is highest in layer V of motor cortex (Murthy and Fetz 1996a; Witham and Baker 2007) and that pyramidal tract layer V neurons can fire rhythmically in the beta frequency (Wetmore and Baker 2004).”

“Early studies of spike synchrony and oscillations in MI addressed the “association hypothesis,” the equivalent of the “binding hypothesis” in the visual system (Murthy and Fetz, 1996a,b).”

“…cortex, during passive viewing of complex visual objects (Freiwald et al., 1998), in the parietal cortex during the preparatory period of a visually guided reaching movement (MacKay and Mendonc¸a, 1995), and in the sensorimotor (Murthy and Fetz, 1996) and motor cortex (Sanes and Donoghue, 1993).”

“ory activity in this frequency range during execution of [26] reported an increase in cross-electrode site synchrony motor tasks in monkeys [29–31].”

“…at a number of loci in the mammalian CNS, notably hippocampus (Czurko et al. 1999; Draguhn et al. 1998), cerebellum (Hartmann and Bower 1998; Mann-Metzer and Yarom 1999), cortex (Crook et al. 1997, 1998; Murthy and Fetz 1996), and thalamocortical circuits (Buzsaki 1991; Llinas et al. 1998).”

“Evidence for the occurrence of bursts versus oscillations in the beta frequency band in particular is accumulating rapidly (Feingold et al., 2015; Jones et al., 2009; Little et al., 2019; Murthy and Fetz, 1996, 1992; Sherman et al., 2016; Shin et al., 2017; Spitzer and Haegens, 2017).”

“…cortical areas have been proposed as a means to bind individual movement segments to produce complex movement patterns (Pfurtscheller et al., 1993; Murthy and Fetz, 1996a,b; MacKay, 1997; Riehle et al., 1997; Donoghue et al., 1998; Lebedev and Wise, 2000; Ohara et al., 2001; Baker et al., 2003).”