Encoding wide-field motion and direction in the central complex of the cockroach, Blaberous discoidalis

Abstract

In the arthropod brain, the central complex (CX) receives various forms of sensory signals and is associated with motor functions, but its precise role in behavior is controversial. The optomotor response is a highly conserved turning behavior directed by visual motion. In tethered cockroaches, 20% procaine injected into the CX reversibly blocked this behavior. We then used multichannel extracellular recording to sample unit activity in the CX in response to wide-field visual motion stimuli, moving either horizontally or vertically at various temporal frequencies. For the 401 units we sampled, we identified five stereotyped response patterns: tonically inhibited or excited responses during motion, phasically inhibited or excited responses at the initiation of motion, and phasically excited responses at the termination of motion. Sixty-seven percent of the units responded to horizontal motion, while only 19% responded to vertical motion. Thirty-eight percent of responding units were directionally selective to horizontal motion. Response type and directional selectivity were sometimes conditional with other stimulus parameters, such as temporal frequency. For instance, 16% of the units that responded tonically to low temporal frequencies responded phasically to high temporal frequencies. In addition, we found that 26% of wide-field motion responding units showed a periodic response that was entrained to the temporal frequency of the stimulus. Our results show a diverse population of neurons within the CX that are variably tuned to wide-field motion parameters. Our behavioral data further suggest that such CX activity is required for effective optomotor responses.

What insects can tell us about the origins of consciousness

“…This function for the CX has been described in locusts and butterflies (Danaus plexippus) but may be common across insect orders (79). Further, in S. gregaria (80), the cockroach Blaberus discoidalis (75), and Drosophila melanogaster (81,82), the CX encodes topographically organized visual information on moving objects and is capable of factoring out the confounding effects of visual motion generated by self-movement from moving objects in the environment (82). In Drosophila, neural activity within the CX encodes the fly's heading relative to visual landmarks in the environment and presumably enables the fly to maintain a course relative to those landmarks (83).…”

“…The effect of Ampulex venom on the cockroach brain is thus to eliminate the capacity of the roach to organize and initiate behavior (73). This example shows that the central brain structures are key for the initiation and direction of movement in cockroaches and crickets (74,75).…”

“…The CX is anatomically variable between insect orders but typically is composed of the central body upper (CBU), central body lower (CBL), and noduli (NO). It has several specializations for processing spatial information corrected for self movement (75,76,83,87). The protocerebrum (P) is an anatomically complicated region.…”

The role of the cerebral ganglia in the venom-induced behavioral manipulation of cockroaches stung by the parasitoid jewel wasp

“…While most CX units show an increase in their firing rate preceding the initiation of locomotion, some show a decrease indicating that the CX is predominantly permissive in walking (Guo and Ritzmann, 2013). In a recently published study, injection of procaine into the CX of Blaberus discoidalis was performed, to investigate its role in optomotor behavior (Kathman et al, 2014); the authors found deficits in optomotor behavior after procaine injection but no significant change in general activity (i.e. walking).…”

“…First, to determine the role that the CX plays in the control of spontaneous walking, we focally injected procaine to the CX to reversibly decrease neuronal activity specifically in this region (Devaud et al, 2007;Gal and Libersat, 2010;Kathman et al, 2014). Compared with the baseline walking duration, cockroaches that were injected with procaine to the CX walked significantly less, if at all, for 30 min after the injections (P<0.05; Fig.…”