Stimulus-induced up states in the dorsal pallium of a weakly electric fish

Abstract

Elliott SB, Maler L. Stimulus-induced up states in the dorsal pallium of a weakly electric fish. J Neurophysiol 114: [2071][2072][2073][2074][2075][2076] 2015.First published August 5, 2015; doi:10.1152/jn.00666.2015.-We investigated the response of putative novelty-detecting neurons in the pallium of an electric fish to electrosensory and acoustic stimuli. Extracellular and whole cell patch recordings were made from neurons in the dorsal pallial nucleus (DD) of Apteronotus leptorhynchus. DD neurons were typically quiescent and exhibited hyperpolarized resting membrane potentials. Stimulation induced, with a variable long latency, rapid though transient depolarization and spike discharge. The transition between resting and depolarized/spiking states resembled the transition to Up states seen in mammalian telencephalic neurons. electrophysiology; up states; weakly electric fish; dorsal pallium ELECTROPHYSIOLOGICAL RECORDINGS from mammalian cortex and striatum have revealed the existence of Up states: the normally quiescent and hyperpolarized membrane potential is interrupted by a brief period of depolarization, increased membrane potential variance, and spike discharge. Up states have been observed both in vivo (Li et al. 2009;Wilson and Kawaguchi 1996) and in vitro (McCormick et al. 2003) and typically occur spontaneously. Up states in cortical pyramidal cells are due to intrinsic cortical dynamics but can be triggered by thalamic input (Maclean et al. 2005) and are controlled in a complex manner by GABAergic inhibition (Mann et al. 2009). It has been difficult to establish a clear link between Up states and external triggering events, and their function remains unknown.Our work focused on Apteronotus leptorhynchus, a weakly electric fish that utilizes its sinusoidal electric organ discharge (EOD) and electroreceptors to communicate, navigate, and locate prey (Chacron et al. 2011;Krahe and Maler 2014;Marsat et al. 2012). The Apteronotus EOD is a constant high-frequency sinusoid, and when two fish are in proximity, their EODs interfere to generate an amplitude modulation (AM) or beat with a frequency equal to the difference of their EOD frequencies. Apteronotus is very sensitive to such AMs and can remember specific beat frequencies for at least 3 days (Harvey-Girard et al. 2010).We recorded from neurons in the dorsal pallium (DD). Neurons in DD have been shown to respond to initial electrosensory beat stimuli and acoustic stimuli with dramatic delayed increases in immediate early gene expression (Egr-1; HarveyGirard et al. 2010). Egr-1 expression also increases in other pallial regions, but to a lesser extent. Egr-1 expression in DD declines to undetectable levels as the fish habituates to a repeatedly presented beat frequency, and expression again increases when novel beat frequencies are presented. This led us to hypothesize that DD was involved in detecting novel stimuli and initiating long-term memory storage of the beat frequency in the large dorsolateral pallium (DL). DD receives glutamergic input from DL...

Hippocampal‐like circuitry in the pallium of an electric fish: Possible substrates for recursive pattern separation and completion

“…Given that DL is essential for spatial learning in goldfish (see above), we propose that DL and DD are involved in pattern separation/completion. We have shown that DDi/DDmg found neurons that could enter a sustained Up state after repeated stimulus presentations; these Up states appeared to be driven by synaptic input (Elliott and Maler, ). We hypothesize that the Up state is due to reverberatory activity within the multiple loops of the DDi recurrent network and the slow NMDA receptor EPSPs (Harvey‐Girard et al, ) which last longer than the maximum loop delay time (50 ms).…”

“…Based on our work we predict that, when the fish receives social stimulation, the DC2 (DD?) region will show very strong increases in Egr‐1 mRNA expression (Harvey‐Girard et al, 2011) as well as a specific electrophysiological response—induction of Up states (Elliott and Maler, ). We believe that A. burtoni is an outstanding system to investigate the neural bases of social learning and, in particular, the interactions of DD and DL in such learning.…”

“…DDi projects to Vd and Vc, components of the striatum (Harvey‐Girard et al, ) and we have previously argued (Sas et al, ) that this region can also be considered as ventral striatum. There is also a functional parallel in that both hilar (Williams et al, ; Larimer and Strowbridge, ) and DDmg/DDi (Elliott and Maler, ) neurons exhibit Up states.…”

Nonstationary Stochastic Dynamics Underlie Spontaneous Transitions between Active and Inactive Behavioral States

“…In support of this hypothesis, a recent study has shown that the recurrent networks of the gymnotiform telencephalon can be induced to switch between up and down states (Elliott and Maler, 2015). Furthermore, work in zebrafish suggests that the orexin and galanin peptidergic systems of the hypothalamus can control the probability of such switches (Prober et al, 2006; Woods et al, 2014).…”

“…Is it mediated only through neuromodulation, as suggested by the induced up states of the telencephalon (Elliott and Maler, 2015), or is there a more direct pathway interacting with the inferred attractor dynamics? In other words, one might want to eventually include closed loop features, going beyond the open-loop perspective that underlies the work presented here, to gain a better understanding of how behavioral state transitions occur in more complex settings.…”