An antennal-derived mechanosensory pathway in the cockroach: descending interneurons as a substrate for evasive behavior

doi:10.1016/0006-8993(90)91623-O

Brain Research

Volume 535, Issue 2, 10 December 1990, Pages 347-352

https://doi.org/10.1016/0006-8993(90)91623-O Get rights and content

Abstract

Large amplitude units responding to intense winds or touch of the antennae were recorded extracellularly from the cervical connectives of the cockroach,Periplaneta americana. Intracellular recording and staining revealed a number of interneurons with cell bodies in one of the head ganglia and large caliber axons descending to thoracic levels. These cells respond to touch of an antenna at very short latencies. The properties of these cells suggest that in the cockroach they may be a substrate for non-GI evasive behavior, especially for responses to predators which are detected by tactile cues.

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Cited by (28)

Possibilities offered by implantable miniaturized cuff-electrodes for insect neurophysiology
2012, Neurocomputing
Citation Excerpt :
Touching one antenna of the insect with a grounded pencil resulted in a strong neuronal response (Fig. 4A). Large amplitude units contributing to this discharge may be analogous to the large amplitude descending mechanosensory interneurons identified in cockroaches [11,30,31]. A wind puff towards the head of the insect evoked a massive neuronal discharge in the nerve recording (Fig. 4B).
Recent advances in microsystems technology led to a miniaturization of cuff-electrodes, which suggests these electrodes not just for long-term neuronal recordings in mammalians, but also in medium-sized insects. In this study we investigated the possibilities offered by cuff-electrodes for neuroethology using insects as a model organism. The implantation in the neck of a tropical bushcricket resulted in high quality extracellular nerve recordings of different units responding to various acoustic, vibratory, optical and mechanical stimuli. In addition, multi-unit nerve activity related to leg movements was recorded in insects walking on a trackball. A drawback of bi-polar nerve recordings obtained during tethered flight was overlay of nerve activity with large amplitude muscle potentials. Interestingly, cuff-electrode recordings were robust to withstand walking and flight activity so that good quality nerve recordings were possible even three days after electrode implantation. Recording multi-unit nerve activity in intact insects required an elaborate spike sorting algorithm in order to discriminate neuronal units responding to external stimuli from background activity. In future, a combination of miniaturized cuff-electrodes and light-weight amplifiers equipped with a wireless transmitter will allow the investigation of neuronal processes underlying natural behavior in freely moving insects. By this means cuff-electrodes may contribute to the development of realistic neuronal models simulating neuronal processes underlying natural insect behavior, such like mate choice and predator avoidance.
Antennal Movements and Mechanoreception: Neurobiology of Active Tactile Sensors
2005, Advances in Insect Physiology
Citation Excerpt :
The indifferent electrode was located in the dorsal abdomen. The effects of the electrical stimulation mimic escape responses described for Periplaneta americana (e.g. Comer et al., 1994; Stierle et al., 1994; see Section 6.1.3.3), but it is unknown whether the underlying neural escape circuit (Burdohan and Comer, 1990; Ye and Comer, 1996) was actually recruited. The rather large variations of the behavioural responses suggest that the electrical stimulation recruited a multitude of circuits.
This chapter focuses on the biology of the antennal tactile sense of insects and crustaceans. It covers the biomechanics, kinematics, and behavioral biology of antennal movements, the peripheral and central neurobiology of antennal mechanoreception, and interdisciplinary aspects of biology and engineering of tactile sensing. The discussion is concentrated on a set of insect model organisms, all of which employ their antennae in active tactile sensing. Work on other species, particularly on decapod crustaceans, is used to complete and contrast the insights from the insect model organisms. The chapter discusses three aspects of the antennal tactile sense that draw on information from various sections and, therefore, require separate treatment. It addresses the behavioral similarities between insect and crustacean antennal tactile sensing, which are particularly remarkable when bearing in mind the morphological differences between these taxa. The chapter also provides a contrast in the categories of passive and active sensing, by relating them to a behavior-based classification of tactile sensing.
Identified nerve cells and insect behavior
2001, Progress in Neurobiology
Studies of insect identified neurons over the past 25 years have provided some of the very best data on sensorimotor integration; tracing information flow from sensory to motor networks. General principles have emerged that have increased the sophistication with which we now understand both sensory processing and motor control. Two overarching themes have emerged from studies of identified sensory interneurons. First, within a species, there are profound differences in neuronal organization associated with both the sex and the social experience of the individual. Second, single neurons exhibit some surprisingly rich examples of computational sophistication in terms of (a) temporal dynamics (coding superimposed upon circadian and shorter-term rhythms), and also (b) what Kenneth Roeder called ‘neural parsimony’: that optimal information can be encoded, and complex acts of sensorimotor coordination can be mediated, by small ensembles of cells. Insect motor systems have proven to be relatively complex, and so studies of their organization typically have not yielded completely defined circuits as are known from some other invertebrates. However, several important findings have emerged. Analysis of neuronal oscillators for rhythmic behavior have delineated a profound influence of sensory feedback on interneuronal circuits: they are not only modulated by feedback, but may be substantially reconfigured. Additionally, insect motor circuits provide potent examples of neuronal restructuring during an organism's lifetime, as well as insights on how circuits have been modified across evolutionary time. Several areas where future advances seem likely to occur include: molecular genetic analyses, neuroecological syntheses, and neuroinformatics — the use of digital resources to organize databases with information on identified nerve cells and behavior.
A motion tracking system for simultaneous recording of rapid locomotion and neural activity from an insect
1995, Journal of Neuroscience Methods
We have adapted techniques for studying the locomotion of tethered insects to analysis of rapid directional movements such as escape behavior. We describe here a computer-based motion tracking system that allows an animal to turn and run as rapidly as it does under free-ranging conditions, and that samples fast enough to accurately reconstruct the movements. Furthermore, we have designed chronic electrodes that allow for simultaneous extracellular recording of the activity of interneurons related to behavior. We used this system to record the escape response of tethered cockroaches, Periplaneta americana, and compared the data with those obtained from high-speed videographic analysis of the same animals under free-ranging conditions. In the motion tracking system, animals were normally responsive to sensory input, and expressed directional escape turning responses. This system allows details of an entire escape response (initial turn and subsequent running) to be quantified. These behavioral details can now be correlated with the discharge of key interneurons on a trial-by-trial basis.
The wind-elicited escape response of cockroaches (Periplaneta americana) is influenced by lesions rostral to the escape circuit
1993, Brain Research
When the escape response of the cockroach (Periplaneta americana) is triggered by wind, it is mediated by the cercal-to-giant interneuron pathway and leg motor circuitry, within the abdominal and thoracic portions of the ventral nerve cord. We have found that a lesion rostral to the thorax (transection of a cervical connective) produces specific changes in wind-evoked escape. Lesioned animals reliably displayed short-latency responses to wind. However, the orientation of the initial turning component of escape was altered and the duration of subsequent running was reduced. Preliminary physiological study suggests that changes in the orientation of escape reflect changes in the integration of wind-sensory signals by thoracic circuitry. These findings imply that rostral centers influence sensorimotor integration underlying wind-evoked escape.
Simulation of adaptive behavior
1991, Current Opinion in Neurobiology

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: This work was supported by NSF Grants No. BNS 86-17393 and No. BNS 89-09051 to C.M.C.

¹: We would like to express our appreciation to Sasha Zill for his donation of piezoelectric crystals. In addition, we thank J. Dowd, A. Keegan, J. Leonard B. McLean, A.D. Murphy, K. Murphy, I. Stierle, and G.T. Stubblefield for providing thoughtful comments on previous versions of this manuscript.

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Brain Research

Abstract

Reference (30)

A silver intensification method for cobalt-filled neurons in wholemount preparations

Brain Research

Search and anemotactic orientation of cockroaches

J. Insect Physiol.

Escape responses following elimination of the giant interneuron pathway in the cockroach,Periplaneta americana

Brain Research

Control of hindlimb posture by wind-sensitive hairs and antennae during locust flight

J. Comp. Physiol.

The tritocerebral commissure giant (TCG) wind-sensitive interneurone in the locust. I. Its activity in straight flight

J. Comp. Physiol.

The dipteran “Giant fibre” pathway: neurons and signals

J. Comp. Physiol.

Initiation of flight by an identified wind sensitive neurone (TCG) in the locust

J. exp. Biol.

The specificity of central nervous projections of locust mechanoreceptors

J. Comp. Neurol.

An inexpensive hot-wire anemometer suitable for behavioral research

Comp. Biochem. Physiol.

Descending pathways carrying wind and tactile sensory information in the nerve cord of the cockroachPeriplaneta americana

Soc. Neurosci. Abstr.

Plurisegmental interneurons carrying antennal-derived tactile sensory information in the cockroach

Soc. Neurosci. Abstr.

Neuroethology

Properties of the escape system of cockroaches during walking

J. Comp. Physiol.

The escape behavior of the cockroachPeriplaneta americana. II. Detection of natural predators by air displacement

J. Comp. Physiol.

Multisensory control of cockroach escape: some predators are detected by antennal and other non-cercal sensory systems

Soc. Neurosci. Abstr.

Cited by (28)

Possibilities offered by implantable miniaturized cuff-electrodes for insect neurophysiology

Antennal Movements and Mechanoreception: Neurobiology of Active Tactile Sensors

Identified nerve cells and insect behavior

A motion tracking system for simultaneous recording of rapid locomotion and neural activity from an insect

The wind-elicited escape response of cockroaches (Periplaneta americana) is influenced by lesions rostral to the escape circuit

Simulation of adaptive behavior