Enhanced sensory sampling precedes self-initiated locomotion in an electric fish

Abstract

Cortical activity precedes self-initiated movements by several seconds in mammals; this observation has led into inquiries on the nature of volition. Preparatory neural activity is known to be associated with decision making and movement planning. Selfinitiated locomotion has been linked to increased active sensory sampling; however, the precise temporal relationship between sensory acquisition and voluntary movement initiation has not been established. Based on long-term monitoring of sensory sampling activity that is readily observable in freely behaving pulse-type electric fish, we show that heightened sensory acquisition precedes spontaneous initiation of swimming. Gymnotus sp. revealed a bimodal distribution of electric organ discharge rate (EODR) demonstrating down-and up-states of sensory sampling and neural activity; movements only occurred during up-states and up-states were initiated before movement onset. EODR during voluntary swimming initiation exhibited greater trial-to-trial variability than the sound-evoked increases in EODR. The sampling variability declined after voluntary movement onset as previously observed for the neural variability associated with decision making in primates. Spontaneous movements occurred randomly without a characteristic timescale, and no significant temporal correlation was found between successive movement intervals. Using statistical analyses of spontaneous exploratory behaviours and associated preparatory sensory sampling increase, we conclude that electric fish exhibit key attributes of volitional movements, and that voluntary behaviours in vertebrates may generally be preceded by increased sensory sampling. Our results suggest that comparative studies of the neural basis of volition may therefore be possible in pulse-type electric fish, given the substantial homologies between the telencephali of teleost fish and mammals.

Subsecond Sensory Modulation of Serotonin Levels in a Primary Sensory Area and Its Relation to Ongoing Communication Behavior in a Weakly Electric Fish

“…This suggests that, even in a “resting state,” there is ongoing neural activity in the brain of these fish that can modulate sensory processing. A similar conclusion was reached for motor activity and EOD discharge in related gymnotiform fish (Jun et al, 2014). …”

“…6), even though gymnotiform fish are known to be very sensitive to sound (Harvey-Girard et al, 2010; Jun et al, 2014). It is therefore possible that distinct populations of DRN neurons innervate different sensory regions of the brain in a modality-specific manner.…”

Waveform sensitivity of electroreceptors in the pulse weakly electric fish Gymnotus omarorum

“…The resulting changes in the transcutaneous electric field are transduced by cutaneous electroreceptors and encoded as train of spikes in primary electroreceptive afferents (Bullock et al, 1961;Fessard and Szabo, 1961;Lissmann, 1958;Szabo and Fessard, 1974;Wright, 1958). This information is further processed in the brain stem (Aumentado-Armstrong et al, 2015;Bell and Maler, 2005;Heiligenberg and Rose, 1985;Kawasaki, 2005) and telencephalon (Harvey Girard et al, 2010;Trinh et al, 2016), giving origin to reflex Post and von der Emde, 1999), stereotyped (Heiligenberg, 1991;Kawasaki, 2005;Moller, 1995) and learned behaviors (Jun et al, 2014;Schumacher et al, 2016;Walton and Moller, 2010).…”

Melatonin Regulates Daily Variations in Electric Behavior Arousal in Two Species of Weakly Electric Fish with Different Social Structures

“…The nocturnal increase of EOD-BR is a common feature among South American weakly electric fish and coincides with a state of nocturnal arousal. In contrast to shortterm novelty responses to sudden changes in prevailing lighting [Capurro, 1994;Post and von der Emde, 1999], a nocturnal increase in EOD-BR is consistent with higher levels of attention, motivation and perceptual efficacy during the active nocturnal phase [Silva et al, 2007;Jun et al, 2014]. There are no previous reports of daily changes in EOD-BR in the wild; however, in laboratory settings, a nocturnal increase in EOD-BR that persists in conditions of constant illumination has been reported in Brachyhypopomus [Stoddard et al, 2007].…”