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Circuit feedback increases activity level of a circuit input through interactions with intrinsic properties.
J Neurophysiol 2017; 118(2):949-963JN

Abstract

Central pattern generator (CPG) motor circuits underlying rhythmic behaviors provide feedback to the projection neuron inputs that drive these circuits. This feedback elicits projection neuron bursting linked to CPG rhythms. The brief periodic interruptions in projection neuron activity in turn influence CPG output, gate sensory input, and enable coordination of multiple target CPGs. However, despite the importance of the projection neuron activity level for circuit output, it remains unknown whether feedback also regulates projection neuron intraburst firing rates. I addressed this issue using identified neurons in the stomatogastric nervous system of the crab, Cancer borealis, a small motor system controlling chewing and filtering of food. Mechanosensory input triggers long-lasting activation of two projection neurons to elicit a chewing rhythm, during which their activity is patterned by circuit feedback. Here I show that feedback increases the intraburst firing rate of only one of the two projection neurons (commissural projection neuron 2: CPN2). Furthermore, this is not a fixed property because the CPN2 intraburst firing rate is decreased instead of increased by feedback when a chewing rhythm is activated by a different modulatory input. I establish that a feedback pathway that does not impact the CPN2 activity level in the control state inhibits CPN2 sufficiently to trigger postinhibitory rebound following mechanosensory stimulation. The rebound increases the CPN2 intraburst firing rate above the rate due only to mechanosensory activation of CPN2. Thus in addition to patterning projection neuron activity, circuit feedback can adjust the intraburst firing rate, demonstrating a novel functional role for circuit feedback to central projection neurons.NEW & NOTEWORTHY Feedback from central pattern generator (CPG) circuits patterns activity of their projection neuron inputs. However, whether the intraburst firing rate between rhythmic feedback inhibition is also impacted by CPG feedback was not known. I establish that CPG feedback can alter the projection neuron intraburst firing rate through interactions with projection neuron intrinsic properties. The contribution of feedback to projection neuron activity level is specific to the modulatory condition, demonstrating a state dependence for this novel role of circuit feedback.

Authors+Show Affiliations

Department of Biology, Miami University, Oxford, Ohio Dawn.Blitz@MiamiOh.edu.

Pub Type(s)

Journal Article
Research Support, U.S. Gov't, Non-P.H.S.

Language

eng

PubMed ID

28469000

Citation

Blitz, Dawn M.. "Circuit Feedback Increases Activity Level of a Circuit Input Through Interactions With Intrinsic Properties." Journal of Neurophysiology, vol. 118, no. 2, 2017, pp. 949-963.
Blitz DM. Circuit feedback increases activity level of a circuit input through interactions with intrinsic properties. J Neurophysiol. 2017;118(2):949-963.
Blitz, D. M. (2017). Circuit feedback increases activity level of a circuit input through interactions with intrinsic properties. Journal of Neurophysiology, 118(2), pp. 949-963. doi:10.1152/jn.00772.2016.
Blitz DM. Circuit Feedback Increases Activity Level of a Circuit Input Through Interactions With Intrinsic Properties. J Neurophysiol. 2017 08 1;118(2):949-963. PubMed PMID: 28469000.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Circuit feedback increases activity level of a circuit input through interactions with intrinsic properties. A1 - Blitz,Dawn M, Y1 - 2017/05/03/ PY - 2016/09/26/received PY - 2017/04/14/revised PY - 2017/04/30/accepted PY - 2017/5/5/pubmed PY - 2018/4/25/medline PY - 2017/5/5/entrez KW - central pattern generator KW - mechanosensory KW - modulation KW - postinhibitory rebound SP - 949 EP - 963 JF - Journal of neurophysiology JO - J. Neurophysiol. VL - 118 IS - 2 N2 - Central pattern generator (CPG) motor circuits underlying rhythmic behaviors provide feedback to the projection neuron inputs that drive these circuits. This feedback elicits projection neuron bursting linked to CPG rhythms. The brief periodic interruptions in projection neuron activity in turn influence CPG output, gate sensory input, and enable coordination of multiple target CPGs. However, despite the importance of the projection neuron activity level for circuit output, it remains unknown whether feedback also regulates projection neuron intraburst firing rates. I addressed this issue using identified neurons in the stomatogastric nervous system of the crab, Cancer borealis, a small motor system controlling chewing and filtering of food. Mechanosensory input triggers long-lasting activation of two projection neurons to elicit a chewing rhythm, during which their activity is patterned by circuit feedback. Here I show that feedback increases the intraburst firing rate of only one of the two projection neurons (commissural projection neuron 2: CPN2). Furthermore, this is not a fixed property because the CPN2 intraburst firing rate is decreased instead of increased by feedback when a chewing rhythm is activated by a different modulatory input. I establish that a feedback pathway that does not impact the CPN2 activity level in the control state inhibits CPN2 sufficiently to trigger postinhibitory rebound following mechanosensory stimulation. The rebound increases the CPN2 intraburst firing rate above the rate due only to mechanosensory activation of CPN2. Thus in addition to patterning projection neuron activity, circuit feedback can adjust the intraburst firing rate, demonstrating a novel functional role for circuit feedback to central projection neurons.NEW & NOTEWORTHY Feedback from central pattern generator (CPG) circuits patterns activity of their projection neuron inputs. However, whether the intraburst firing rate between rhythmic feedback inhibition is also impacted by CPG feedback was not known. I establish that CPG feedback can alter the projection neuron intraburst firing rate through interactions with projection neuron intrinsic properties. The contribution of feedback to projection neuron activity level is specific to the modulatory condition, demonstrating a state dependence for this novel role of circuit feedback. SN - 1522-1598 UR - https://www.unboundmedicine.com/medline/citation/28469000/Circuit_feedback_increases_activity_level_of_a_circuit_input_through_interactions_with_intrinsic_properties_ L2 - http://www.physiology.org/doi/full/10.1152/jn.00772.2016?url_ver=Z39.88-2003&rfr_id=ori:rid:crossref.org&rfr_dat=cr_pub=pubmed DB - PRIME DP - Unbound Medicine ER -