Species-specific behavioral patterns correlate with differences in synaptic connections between homologous mechanosensory neurons

Abstract

We characterized the behavioral responses of two leech species, Hirudo verbana and Erpobdella obscura, to mechanical skin stimulation and examined the interactions between the pressure mechanosensory neurons (P cells) that innervate the skin. To quantify behavioral responses, we stimulated both intact leeches and isolated body wall preparations from the two species. In response to mechanical stimulation, Hirudo showed local bending behavior, in which the body wall shortened only on the side of the stimulation. Erpobdella, in contrast, contracted both sides of the body in response to touch. To investigate the neuronal basis for this behavioral difference, we studied the interactions between P cells. Each midbody ganglion has four P cells; each cell innervates a different quadrant of the body wall. Consistent with local bending, activating any one P cell in Hirudo elicited polysynaptic inhibitory potentials in the other P cells. In contrast, the P cells in Erpobdella had excitatory polysynaptic connections, consistent with the segment-wide contraction observed in this species. In addition, activating individual P cells caused asymmetrical body wall contractions in Hirudo and symmetrical body wall contractions in Erpobdella. These results suggest that the different behavioral responses in Erpobdella and Hirudo are partly mediated by interactions among mechanosensory cells.

Developmentally regulated multisensory integration for prey localization in the medicinal leech

“…Such a change could result in an increase in the influence of mechanosensors because they are both increasing in sensitivity and size during this time period while the visual system is not changing. Alternatively, the change could occur as the result of a change in synaptic strength of either excitatory or inhibitory connections (Baltzley et al, 2010;Chiang et al, 2006;Lockery et al, 1989). Lastly, a neuromodulatory mechanism could be responsible.…”

“…Lastly, a neuromodulatory mechanism could be responsible. Such mechanisms have been noted in central pattern generators (CPGs) in many animal species and have been hypothesized to allow for CPG-controlled behavior to adapt to conditions surrounding the animal at that moment, developmental stage or evolutionary stage (Baltzley et al, 2010;Briggman and Kristan, 2008;Crisp and Mesce, 2003;Fenelon et al, 1999;Fenelon et al, 2004;Gaudry and Kristan, 2009;Katz, 1998;Lockery and Kristan, 1991;Newcomb and Katz, 2007). Interestingly, in most of these examples the excitability of the system is modulated by serotonin, which in Hirudo is known to result in the decreased sensitivity of mechanosensors during feeding (Gaudry and Kristan, 2009;Gaudry and Kristan, 2010).…”

Behavioral Analysis of Substrate Texture Preference in a Leech,Helobdella austinensis

“…The mechanosensory system of the leech provides some possibilities about how these mechanisms might be implemented. (NB: Most of this information has been garnered from work on other species than Helobdella , primarily 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65 European medicinal leeches, but mechanosensory neurons have been recorded in many other leech species Kuwada and Kramer 1983;Lent 1985;Nusbaum and Kristan 1986;Baltzley et al 2010) without significant differences among the species.) In each of the leech's 21 midbody segments there are 3 pairs of T cells (respond to very light touch), 2 pairs of P cells (respond to pressure on the skin), and 2 pairs of N cells (respond to strong mechanical, chemical, and thermal stimuli) (Nicholls and Baylor 1968;Carlton and McVean 1995).…”

“…Behavioral comparisons across leech species have revealed intriguing differences as well. For example, activation of P cells in the midbody of H. verbana produces a local bending response away from the site of stimulation whereas the same P cell activation in E. obscura causes them to roll themselves into a tight coil (Baltzley et al 2010). In addition, activation of P or N cells in the back end of most leech species normally initiates locomotor behavior (crawling or swimming) (Kristan 1982;Palmer et al 2014) but these responses are inhibited by feeding behavior specifically among various sanguivorous (blood-sucking) species, for which feeding opportunities are rare and of high energetic value, but not in predaceous species, for which feeding opportunities are more common and less valuable energetically .…”

Artificial Synaptic Rewiring Demonstrates that Distinct Neural Circuit Configurations Underlie Homologous Behaviors

“…In the stomatogastric nervous system of decapod crustaceans, there are differences between crab and spiny lobster in electrical connections among homologous motor neurons; however, the pyloric motor pattern is highly conserved [20,21]. In leeches, differences in the polarity of synaptic connections among the mechanosensory P cells underlie the difference in behavioral expressions in two species [22]. Differences in synaptic connectivity among homologous neurons have also been reported in two species of nematode with different feeding behaviors [23].…”