Christopher M. Comer

Somatosensory organization and behavior in naked mole‐rats: II. Peripheral structures, innervation, and selective lack of neuropeptides associated with thermoregulation and pain

African naked mole‐rats are subterranean rodents that have a robust orienting response to stimulation of unique vibrissa‐like body hairs that are widely spaced over an otherwise hairless skin. To determine whether these large body hairs have a specialized organization similar to facial vibrissae, the structure and innervation of facial vibrissa follicles, body hair follicles, and intervening skin in naked mole‐rats was compared with that in rats and a furred African mole‐rat species (the common mole‐rat). Immunofluorescence and lectin‐binding analyses revealed that the body hair follicles in naked mole‐rats were exceptionally large and well innervated, similar to guard hairs of furred species. However, these body vibrissae lacked the anatomic specializations and unique types of innervation affiliated with follicle sinus complexes of facial vibrissae. In contrast to the furred species, naked mole‐rats had a paucity of Aβ‐fiber Merkel endings at all peripheral locations. Naked mole‐rats also were completely lacking in cutaneous C‐fibers immunoreactive for substance P and calcitonin gene‐related peptide. In contrast, the hairless skin of the naked mole‐rats had an exceptional abundance of presumptive Aδ‐fibers. The unusual features of the cutaneous innervation in naked mole‐rats are presumably adaptations to their subterranean environment and that they are the only known poikilothermic mammal. The features of this mammalian model system provide unique opportunities to discriminate mechanisms related to tactile spatial orientation, vascular regulation, and nociception. J. Comp. Neurol. 465:104–120, 2003.

Somatosensory Organization and Behavior in Naked Mole-Rats I: Vibrissa-Like Body Hairs Comprise a Sensory Array That Mediates Orientation to Tactile Stimuli

Orientation guided by mechanosensory stimuli is a fundamental behavior that has been analyzed most effectively in simple systems, but has been difficult to assess in mammals. This study demonstrates that sparsely distributed sensory ‘hairs’ on the body of naked mole-rats provide an ideal detector array for the assessment of touch guided orienting behavior. Naked mole-rats are fully subterranean rodents that are functionally blind and lack fur. About 40 tactile hairs (resembling facial vibrissae) are found on each side of the body, and they are systematically organized in a grid-like pattern from head to tail. Deflection of a single body hair triggered a highly accurate orientation of the snout toward the point of stimulation, thus topographically organized motor behavior can be elicited from this sensory array. This orienting behavior is specific to the body hair system: touch of intervening skin evoked responses less reliably, and observed responses were not topographically organized. Orientation elicited from this array was accurate regardless of the head-to-body position at the time of hair stimulation indicating that the orienting motor score takes relative head position into account. The consistent pattern of these hairs coupled with robust orienting behavior indicates that this mammalian model provides an appropriately simple system for analyzing the neuronal basis of sensorimotor integration involved in tactile orienting behavior.

The antennal system and cockroach evasive behavior. I. Roles for visual and mechanosensory cues in the response

Cockroaches escape from predators by turning and then running. This behavior can be elicited when stimuli deflect one of the rostrally located and highly mobile antennae. We analyzed the behavior of cockroaches, under free-ranging conditions with videography or tethered in a motion tracking system, to determine (1) how antennal positional dynamics influence escape turning, and (2) if visual cues have any influence on antennal mediated escape. The spatial orientation of the long antennal flagellum at the time of tactile stimulation affected the direction of resultant escape turns. However, the sign of flagellar displacement caused by touch stimuli, whether it was deflected medially or laterally for example, did not affect the directionality of turns. Responsiveness to touch stimuli, and escape turn performance, were not altered by blocking vision. However, because cockroaches first orient an antenna toward stimuli entering the peripheral visual field, turn direction can be indirectly influenced by visual input. Finally, when vision was blocked, the run phase of escape responses displayed reduced average velocities and distances traveled. Our results suggest that tactile and visual influences are integrated with previously known wind-sensory mechanisms to achieve multisensory control of the full escape response.

Multisensory control of escape in the cockroach Periplaneta americana

Abstract1.All giant interneurons (GIs) were ablated from the nerve cord of cockroaches by electrocautery, and escape behavior was analyzed with high-speed videography. Animals with ablations retained the ability to produce wind-triggered escape, although response latency was increased (Table 1, Fig. 4). Subsequent lesions suggested that these non-GI responses depended in part on receptors associated with the antennae.2.Antennal and cereal systems were compared by analyzing escape responses after amputating either cerci or antennae. With standard wind stimuli (high peak velocity) animals responded after either lesion. With lower intensity winds, animals lost their ability to respond after cereal removal (Fig. 6).3.Removal of antennae did not cause significant changes in behavioral latency, but in the absence of cerci, animals responded at longer latencies than normal (Fig. 7).4.The cercal-to-GI system can mediate short latency responses to high or low intensity winds, while the antennal system is responsive to high intensity winds only and operates at relatively longer latencies. These conclusions drawn from lesioned animals were confirmed in intact animals with restricted wind targeting the cerci or antennae only (Fig. 9).5.The antennae do not represent a primary wind-sensory system, but may have a direct mechanosensory role in escape.

Features of visual function in the naked mole-rat Heterocephalus glaber

The eyes and visual capacity of the naked mole-rat, Heterocephalus glaber, a subterranean rodent, were evaluated using anatomical, biochemical, and functional assays, and compared to other rodents of similar body size (mouse and gerbil). The eye is small compared to mouse, yet possesses cornea, lens, and retina with typical mammalian organization. The optic nerve cross-sectional area and fiber density are ~10% and ~50% that of gerbil, respectively. Levels per unit retinal area of 11-cis and all-trans retinal, derivatives of vitamin A associated with the visual cycle, are comparable to mouse. The corneal electroretinogram (ERG) exhibits early and late negative components that scale with flash strength; raising the body temperature of this poikilothermic animal from 30°C (normal for H. glaber ) to 37°C (normal for mouse) revealed an ERG response with typically mammalian features, but greatly attenuated and with slower kinetics. Leaving the nest chamber was a behavior correlated with light onset displayed preferentially by breeding females. Optical models of five mole-rat eyes suggest reasonable, but variable, image formation at the retina, possibly related to age. Results are consistent with amorphous light detection, possibly useful for circadian entrainment or escape behavior in the event of tunnel breeches.

VISUALLY ELICITED TURNING BEHAVIOR IN RANA PIPIENS : COMPARATIVE ORGANIZATION AND NEURAL CONTROL OF ESCAPE AND PREY CAPTURE

High-speed videography was used to describe the initial turning movement of visually triggered escape in frogs and to compare it with the initial turn of frog prey capture behavior. These two types of turning had some general similarities, e.g. turn duration and peak velocity were positively correlated with turn angle. However, there were kinematic differences: for turns of a given angular amplitude, escape turns consistently demonstrated shorter duration and higher peak velocity than prey capture turns. There also were differences predictably matched to stimulus angles; escape turn angles were more variably related to stimulus angles. Both turning movements are believed to depend upon the optic tectum. However, given the observed differences in kinematics and spatial organization, we used lesion experiments to determine if distinct tectal efferent pathways subserve turning under each circumstance. Large unilateral lesions of the brainstem simultaneously disrupted both types of turning. However, smaller laterally placed lesions disrupted escape turning without disrupting prey capture turns. The kinematic differences in combination with the lesion results support the idea that the post-tectal circuitry for visually elicited turning movements is based upon separate descending pathways that control turning toward prey and turning away from threat.

Collision avoidance by running insects: antennal guidance in cockroaches

SUMMARY Cockroaches were observed with videographic methods as escape running was initiated, but with obstacles in the path of their run. The goal was to determine the repertoire of possible responses to obstacles and the sensory cues used to trigger the responses. Intact cockroaches collided with obstacles on only about 10% of trials. The most common collision avoidance strategy was simply to stop running prior to impact. However, occasionally animals moved vertically and climbed over the barrier, or turned and navigated an edge of the obstacle, or completely reversed run direction. The avoidance strategies chosen depended on the size and configuration of the obstacle. Tests for the use of vision in detecting obstacles showed that its role, if any, is small. However, all manipulations that altered the antennal system changed behavior in a way consistent with the hypothesis that antennal mechanosensation plays a major role in collision avoidance. For example, reducing antennal length, or severing the main antennal nerve without altering the length produced significant increases in the frequency of collisions. Tests with tethered insects showed that (1) the antennae are preferentially directed forward as animals run, and (2) nearly simultaneous contact with both antennae is required to make the cockroach stop. Our data indicate that running cockroaches employ strategies that set their sensorimotor systems in a mode of readiness to deal with obstacles and they suggest that sensory information about the presence and configuration of obstacles is used to make choices, at very short latencies, about how to respond to obstructions.

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

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.

Escape turning behavior of the cockroach

Summary1.The wind-elicited escape turning behavior of cockroaches (Periplaneta americana) receiving various unilateral lesions of the abdominal nervous system was observed using high-speed videography. Lesions were intended to cause an imbalance of wind sensory information in the cercalto-GI pathway (Fig. 1).2.In adult cockroaches unilateral cereal ablation produced a partial shift in the direction of escape turning: a tendency to turn inappropriately toward, rather than away from, wind stimuli on the side of the ablation. However, hemisection of the abdominal nerve cord in adults produced a complete shift in the direction of turning: virtually every turn was directed toward winds on the side of the lesion. In both cases winds from the intact side still elicited turns that were appropriately directed away from the stimulus (Figs. 5, 6 and 8). Hemisection of the abdominal cord in nymphs also shifted the direction of escape turning, but not to the extent seen in adults (Figs. 7 and 8).3.The orientation of an escape turn is determined not only by its direction but also by its angular amplitude. Rear winds normally elicit small angle turns, frontal winds also elicit larger angle turns (Fig. 9). Unilateral lesions can disrupt the direction of turning without necessarily disrupting the normal patterning of turn amplitude (Fig. 10).4.These results are interpreted in terms of the idea that a bilateral comparison of wind evoked GI activity determines the direction of an escape turn. This type of neural integration does not appear to be essential, however, for the determination of the amplitude of an escape turn.

Active touch in orthopteroid insects: behaviours, multisensory substrates and evolution

Orthopteroid insects (cockroaches, crickets, locusts and related species) allow examination of active sensory processing in a comparative framework. Some orthopteroids possess long, mobile antennae endowed with many chemo- and mechanoreceptors. When the antennae are touched, an animals response depends upon the identity of the stimulus. For example, contact with a predator may lead to escape, but contact with a conspecific may usually not. Active touch of an approaching object influences the likelihood that a discrimination of identity will be made. Using cockroaches, we have identified specific descending mechanosensory interneurons that trigger antennal-mediated escape. Crucial sensory input to these cells comes from chordotonal organs within the antennal base. However, information from other receptors on the base or the long antennal flagellum allows active touch to modulate escape probability based on stimulus identity. This is conveyed, at least to some extent, by textural information. Guidance of the antennae in active exploration depends on visual information. Some of the visual interneurons and the motor neurons necessary for visuomotor control have been identified. Comparisons across Orthoptera suggest an evolutionary model where subtle changes in the architecture of interneurons, and of sensorimotor control loops, may explain differing levels of vision–touch interaction in the active guidance of behaviour.