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Abstract
To study cerebellar activity during learning, we made whole-cell recordings from larval zebrafish Purkinje cells while monitoring fictive swimming during associative conditioning. Fish learned to swim in response to visual stimulation preceding tactile stimulation of the tail. Learning was abolished by cerebellar ablation. All Purkinje cells showed task-related activity. Based on how many complex spikes emerged during learned swimming, they were classified as multiple, single, or zero complex spike (MCS, SCS, ZCS) cells. With learning, MCS and ZCS cells developed increased climbing fiber (MCS) or parallel fiber (ZCS) input during visual stimulation; SCS cells fired complex spikes associated with learned swimming episodes. The categories correlated with location. Optogenetically suppressing simple spikes only during visual stimulation demonstrated that simple spikes are required for acquisition and early stages of expression of learned responses, but not their maintenance, consistent with a transient, instructive role for simple spikes during cerebellar learning in larval zebrafish.
Highlights
The activity of cerebellar Purkinje cells regulates both practiced and new movements (Thach, 1968; McCormick and Thompson, 1984; Medina et al, 2000; Mauk et al, 2014)
With the goal of testing how Purkinje neurons contribute to associative learning in larval zebrafish, we first investigated whether they displayed consistent synaptic responses and firing patterns during sensory stimuli and/or fictive swimming
This activity was evident as clusters of EPSCs (Figure 1E and H); in current clamp these events could summate to produce long-lasting depolarizations, typically with simple spikes riding on top (Figure 1I)
Summary
The activity of cerebellar Purkinje cells regulates both practiced and new movements (Thach, 1968; McCormick and Thompson, 1984; Medina et al, 2000; Mauk et al, 2014). Complex spikes arise from synaptic input from climbing fibers and can induce plasticity of other afferents to Purkinje cells, thereby serving as teaching and/or error signals during motor learning (Gilbert and Thach, 1977; Mauk et al, 1986; Medina et al, 2002; Ohmae and Medina, 2015) Despite their shared modes of action potential firing, Purkinje cells in different cerebellar regions contribute differentially to behaviors, owing to their anatomical connections, including distinct innervation patterns by mossy fiber-granule cell pathways (Bower et al, 1981; Bower and Woolston, 1983; Garwicz et al, 1998) and inferior olivary modules (Voogd and Glickstein, 1998; Sugihara and Shinoda, 2004; Ruigrok, 2011; Cerminara and Apps, 2011), as well as different targets.
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