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Descending control of turning behavior in the cockroach, Blaberus discoidalis

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Abstract

Legged locomotion has evolved as the most effective form of movement through unpredictable and tortuous environments. Upon encountering an obstacle, an animal must evaluate the object with its sense organs then use the information it acquires to direct appropriate transitional behaviors, such as turning. Previous studies using genetic and surgical lesions implicate the central body complex (CBC) in control of such transitional behaviors of various insects. In this study, lesions of the CBC and surrounding brain regions were used to examine the effects of damage on turning in free-moving and tethered cockroaches. Lesions were performed either as sagittal incisions or by inserting small pieces of foil into regions of the brain. Locomotor behaviors of intact and lesioned animals were compared using high speed video and kinematic analysis. The lesions locations were determined through histological methods. Sagittal lesions to the CBC often result in continuous or incorrect turns. Foil lesions in the CBC also increase the probability that individuals will show turning deficits. The location and degree of the lesion had a strong effect on the animal’s ability to turn. These data strongly suggest that the CBC mediates the effects of head sense organs that produce changes in the direction of walking.

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Abbreviations

SOG:

Suboesophageal ganglion

NL:

Neck connective lesion

CoCL:

Circumoesophageal connective lesion

CBC:

Central body complex

CoM:

Center of mass

FB:

Fan-shaped body

PB:

Protocerebral bridge

EB:

Ellipsoid body

MB:

Mushroom body

MR:

Motor reporters

AF:

Afferent pathways

MMI:

Multimodal interneurons

LAL:

Lateral accessory lobe

PI:

Pars intercerebralis

References

  • Agresti A (1990) Categorical data analysis. Wiley, New York

    Google Scholar 

  • Blaesing B, Cruse H (2004a) Stick insect locomotion in a complex environment: climbing over large gaps. J Exp Biol 207:1273–1286

    Article  Google Scholar 

  • Blaesing B, Cruse H (2004b) Mechanisms of stick insect locomotion in a gap-crossing paradigm. J Comp Physiol A 190:173–183

    Article  Google Scholar 

  • Bodian D (1936) A new method for staining nerve fibers and nerve endings in mounted paraffin sections. Anat Rec 65:89–97

    Article  Google Scholar 

  • Büschges A, Ramirez JM, Pearson KG (1992a) Reorganization of sensory regulation of locust flight after partial deafferentation. J Neurobiol 23:31–43

    Article  Google Scholar 

  • Büschges A, Ramirez JM, Driesang R, Pearson KG (1992b) Connections of the forewing tegulae in the locust flight system and their modification following partial deafferentation. J Neurobiol 23:44–60

    Article  Google Scholar 

  • Callaerts P, Leng S, Clements J, Benassayag C, Cribbs D, Kang YY, Walldorf U, Fischbach KF, Strauss R (2001) Drosophila Pax-6/eyeless is essential for normal adult brain structure and function. J Neurobiol 46:73–88

    Article  PubMed  CAS  Google Scholar 

  • Camhi J, Johnson E (1999) High-frequency steering maneuvers mediated by tactile cues: antennal wall following in the cockroach. J Exp Biol 202:631–643

    PubMed  CAS  Google Scholar 

  • Cruse H (2002) The functional sense of central oscillations in walking. Biol Cybern 86:271–280

    Article  PubMed  CAS  Google Scholar 

  • Dürr V, Ebeling W (2005) The behavioural transition from straight to curve walking: kinetics of leg movement parameters and the initiation of turning. J Exp Biol 208:2237–2252

    Article  PubMed  Google Scholar 

  • Homberg U (1987) Structure and functions of the central complex in insects. In: Gupta AP (ed) Arthropod brain: its evolution, development, structure and functions. Wiley, New York, pp 347–367

    Google Scholar 

  • Homberg U (1991) Neuroarchitecture of the central complex in the brain of the locust Schistocerca gregaria and S. americana as revealed by serotonin immunocytochemistry. J Comp Neurol 303:245–254

    Article  PubMed  CAS  Google Scholar 

  • Homberg U (1994) Flight-correlated activity changes in neurons of the lateral accessory lobes in the brain of the locust Schistocerca gregaria. J Comp Physiol A 175:597–610

    Article  Google Scholar 

  • Homberg U, Kingan TG, Hildebrand JG (1987) Immunocytochemistry of GABA in the brain and suboesophageal ganglion of Manduca sexta. Cell Tissue Res 248:1–24

    Article  PubMed  CAS  Google Scholar 

  • Homberg U, Kingan TG, Hildebrand JG (1990) Distribution of FMRFamide-like immunoreactivity in the brain and suboesophageal ganglion of the sphinx moth Manduca sexta and colocalization with SCPB-, BPP-, and GABA-like immunoreactivity. Cell Tissue Res 259:401–419

    Article  PubMed  CAS  Google Scholar 

  • Homberg U, Vitzthum H, Muller M, Binkle U (1999) Immunocytochemistry of GABA in the central complex of the locust Schistocerca gregaria: identification of immunoreactive neurons and colocalization with neuropeptides. J Comp Neurol 409:495–507

    Article  PubMed  CAS  Google Scholar 

  • Huber F (1960) Untersuchungen uber die funtion des entralnervensystems und insbesondere des gehirnes bei der fortbewegung und der lauterzeugung der Grillen. Zeit Vergleich Physiol 44:60–132

    Article  Google Scholar 

  • Jindrich DL, Full RJ (1999) Many-legged maneuverability: dynamics of turning in hexapods. J Exp Biol 202:1603–1623

    PubMed  Google Scholar 

  • Jindrich DL, Full RJ (2002) Dynamic stabilization of rapid hexapedal locomotion. J Exp Biol 205:2803–2823

    PubMed  Google Scholar 

  • Kanzaki R, Arbas EA, Hildebrand JG (1991) Physiology and morphology of descending neurons in pheromone-processing olfactory pathways in the male moth Manduca sexta. J Comp Physiol A 169:1–14

    Article  PubMed  CAS  Google Scholar 

  • Kien J (1983) The initiation and maintenance of walking in the locust: an alternative to the command concept. Proc R Soc Lond B Biol Sci 219:137–174

    Article  Google Scholar 

  • Loesel R, Homberg U (1999) Histamine-immunoreactive neurons in the brain of the cockroach Leucophaea maderae. Brain Res 842:408–418

    Article  PubMed  CAS  Google Scholar 

  • Loesel R, Nassel DR, Strausfeld N (2002) Common design in a unique midline neuropil in the brains of arthropods. Arthro Struct Dev 31:77–91

    Article  Google Scholar 

  • Mantel N, Haenszel W (1959) Statistical aspects of the analysis of data from retrospective studies of disease. J Natl Cancer Inst 22:718–748

    Google Scholar 

  • Martin J, Raabe T, Heisenberg M (1999) Central complex substructures are required for the maintenance of locomotor activity in Drosophila melanogaster. J Comp Physiol A 185:277–288

    Article  PubMed  CAS  Google Scholar 

  • Mishima F, Kanzaki R (1999) Physiological and morphological characterization of olfactory descending interneurons of the male silkworm moth, Bombyx mori. J Comp Physiol A 184:143–160

    Article  Google Scholar 

  • Mizunami M, Weibrecht JM, Strausfeld NJ (1998) Mushroom bodies of the cockroach: their participation in place memory. J Comp Neurol 402:520–537

    Article  PubMed  CAS  Google Scholar 

  • Mu L, Ritzmann RE (2005) Kinematics and motor activity during tethered walking and turning in the cockroach, Blaberus discoidalis. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 191:1037–1054

    Article  PubMed  Google Scholar 

  • Muller M, Homberg U, Kuhn A (1997) Neuroarchitecture of the lower division of the central body in the brain of the locust (Schistocerca gregaria). Cell Tissue Res 288:159–176

    Article  PubMed  CAS  Google Scholar 

  • Okada R, Sakura M, Mizunami M (2003) Distribution of dendrites of descending neurons and its implications for the basic organization of the cockroach brain. J Comp Neurol 458:158–174

    Article  PubMed  Google Scholar 

  • Pearson K (2000) Neural adaptation in the generation of rhythmic behavior. Ann Rev Physiol 62:723–753

    Article  CAS  Google Scholar 

  • Pielage J, Steffes G, Lau DC, Parente BA, Crews ST, Strauss R, Klambt C (2002) Novel behavioral and developmental defects associated with Drosophila single-minded. Dev Biol 249:283–299

    Article  PubMed  CAS  Google Scholar 

  • Ridgel AL, Ritzmann RE (2005) Effects of neck and circumoesophageal connective lesions on posture and locomotion in the cockroach. J Comp Physiol A 191:559–573

    Article  Google Scholar 

  • Ritzmann RE, Quinn RD, Fischer MS (2004) Convergent evolution and locomotion through complex terrain by insects, vertebrates and robots. Arthro Struct Dev 33:361–379

    Article  Google Scholar 

  • Ritzmann RE, Pollack AJ, Archinal J, Ridgel AL, Quinn RD (2005) Descending control of body attitude in the cockroach, Blaberus discoidalis and its role in incline climbing. J Comp Physiol A 191:253–264

    Article  Google Scholar 

  • Roeder K (1937) The control of tonus and locomotor activity in the praying mantis (Mantis religiosa L.). J Exp Biol 76:353–374

    Google Scholar 

  • Strausfeld NJ (1998) Crustacean-insect relationships: the use of brain characters to derive phylogeny amongst segmented invertebrates. Brain Behav Evol 52:186–206

    Article  PubMed  CAS  Google Scholar 

  • Strausfeld NJ (1999) A brain region in insects that supervises walking. Prog Brain Res 123:273–284

    Article  PubMed  CAS  Google Scholar 

  • Strausfeld NJ (2003) Brain and optic lobes. In: Resh VH, Carde RT (eds) Encyclopedia of Insects. Academic, New York, pp 137–147

    Google Scholar 

  • Strauss R (2002) The central complex and the genetic dissection of locomotor behaviour. Curr Opin Neurobiol 12:633–638

    Article  PubMed  CAS  Google Scholar 

  • Strauss R, Heisenberg M (1990) Coordination of legs during straight walking and turning in Drosophila melanogaster. J Comp Physiol A 167:403–412

    Article  PubMed  CAS  Google Scholar 

  • Strauss R, Heisenberg M (1993) A higher control center of locomotor behavior in the Drosophila brain. J Neurosci 13:1852–1861

    PubMed  CAS  Google Scholar 

  • Strauss R, Hanesch U, Kinkelin M, Wolf R, Heisenberg M (1992) No-bridge of Drosophila melanogaster: portrait of a structural brain mutant of the central complex. J Neurogenet 8:125–155

    PubMed  CAS  Google Scholar 

  • Tryba AK, Ritzmann RE (2000a) Multi-joint coordination during walking and foothold searching in the Blaberus cockroach. II. Extensor motor neuron pattern. J Neurophysiol 83:3337–3350

    CAS  Google Scholar 

  • Tryba AK, Ritzmann RE (2000b) Multi-joint coordination during walking and foothold searching in the Blaberus cockroach. I. Kinematics and electromyograms. J Neurophysiol 83:3323–3336

    CAS  Google Scholar 

  • Varnam CJ, Strauss R, Belle JS, Sokolowski MB (1996) Larval behavior of Drosophila central complex mutants: interactions between no bridge, foraging, and Chaser. J Neurogenet 11:99–115

    PubMed  CAS  Google Scholar 

  • Vitzthum H, Muller M, Homberg U (2002) Neurons of the central complex of the locust Schistocerca gregaria are sensitive to polarized light. J Neurosci 22:1114–1125

    PubMed  CAS  Google Scholar 

  • Watson JT, Ritzmann RE, Zill SN, Pollack AJ (2002) Control of obstacle climbing in the cockroach, Blaberus discoidalis. I. Kinematics. J Comp Physiol A 188:39–53

    Article  Google Scholar 

  • Whelan PJ, Pearson KG (1997) Plasticity in reflex pathways controlling stepping in the cat. J Neurophysiol 78:1643–1650

    Google Scholar 

Download references

Acknowledgments

The authors thank Dr. Nicholas Strausfeld for help with early stages of this project and Dr. Jay Alexander for help with statistical tests. This work is supported by Eglin AFB Grant F08630-03-01-0003 and NSF Grant IOB-0516587 to RER.

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Correspondence to Roy E. Ritzmann.

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Ridgel, A.L., Alexander, B.E. & Ritzmann, R.E. Descending control of turning behavior in the cockroach, Blaberus discoidalis . J Comp Physiol A 193, 385–402 (2007). https://doi.org/10.1007/s00359-006-0193-7

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  • DOI: https://doi.org/10.1007/s00359-006-0193-7

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