Modulation of wind sensitivity in thoracic interneurons during cricket escape behavior (original) (raw)
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Brain Research, 1991
Research on the escape system of the cockroach has focused upon the role of giant interneurons in conveying information on wind stimulation from the cerci located on the abdomen to motor control centers in the thoracic ganglia. In the thoracic ganglia the ventral giant interneurons connect to a population of interganglionic interneurons referred to as type A thoracic interneurons. In this paper we have tested the type A interneurons for additional sensory inputs in the absence of ventral giant interneuron activity. We find that the cells that receive ventral giant interneuron activity are also influenced by a variety of additional sensory inputs; wind mediated activity in a pathway that descends from the head, tactile inputs from several loci, auditory stimuli and light responses. Moreover, behavioral observations indicate that at least some of these activities can alter the escape movements. The results suggest that these interneurons serve as a site of convergence for numerous types of sensory activity. They further suggest that the escape system is capable of responding to directional wind information encoded in the ventral giant interneurons in the context of a wealth of additional information.
Journal of Comparative Physiology A: Sensory, Neural, and Behavioral Physiology, 1998
Ascending interneurones of the terminal ganglion of orthopterous insects are known to carry information on wind stimuli perceived by cercal receptors to thoracic and cephalic ganglia. Neurones of these anterior ganglia control evasive walking behaviour. We demonstrate that current injection into individual windsensitive local non-spiking interneurones and ascending giant interneurones of the terminal ganglion can in¯uence the orientation behaviour of walking crickets. To induce a change of turning during``wind pu stimulation'' by current injection into the lateral giant interneurone, its spike activity has to be modi®ed by at least 100%. In 5 of 12 dierent types of non-spiking interneurones a moderate shift of the membrane potential results in a change of the mean speed of rotation and/or the frequency of turns. All preparations tested with dierent amounts of current injection showed a proportional change of turning frequency. Normally, the turning behaviour is evasive with respect to the wind source. During current injection this dependence is preserved, but the general orientation is readjusted. Taking into account known connections between some of these interneurones and ascending neurones the tested wind-sensitive local non-spiking interneurones of the terminal ganglion are likely to impose an oset on the mean direction of orientation controlled by cephalic and thoracic neuronal networks.
Responses of cricket cercal interneurons to realistic naturalistic stimuli in the field
Journal of Experimental Biology, 2012
The ability of the insect cercal system to detect approaching predators has been studied extensively in the laboratory and in the field. Some previous studies have assessed the extent to which sensory noise affects the operational characteristics of the cercal system, but these studies have only been carried out in laboratory settings using white noise stimuli of unrealistic nature. Using a piston mimicking the natural airflow of an approaching predator, we recorded the neural activity through the abdominal connectives from the terminal abdominal ganglion of freely moving wood crickets (Nemobius sylvestris) in a semi-field situation. A cluster analysis of spike amplitudes revealed six clusters, or ʻunitsʼ, corresponding to six different subsets of cercal interneurons. No spontaneous activity was recorded for the units of larger amplitude, reinforcing the idea they correspond to the largest giant interneurons. Many of the cercal units are already activated by background noise, sometimes only weakly, and the approach of a predator is signaled by an increase in their activity, in particular for the larger-amplitude units. A scaling law predicts that the cumulative number of spikes is a function of the velocity of the flow perceived at the rear of the cricket, including a multiplicative factor that increases linearly with piston velocity. We discuss the implications of this finding in terms of how the cricket might infer the imminence and nature of a predatory attack.
Journal of Comparative Physiology A, 1988
1. The cockroach PeripIaneta americana can modify the sensory activity received by its central nervous system from the cerci, paired abdominal wind-responsive appendages. Medial displacement of the cerci produces a reduction in the number of sensory action potentials (AP's) elicited by a wind stimulus (Fig. 2) (Libersat et al. 1987; Goldstein and Camhi 1988). This movement occurs naturally, for example during flying. 2. This sensory reduction is present when measured as the integral of extracellularly recorded activity as well as when counting the number of AP's larger than a threshold voltage just larger than the background noise (Fig. 2 C). 3. Histological results confirm prior physiological experiments suggesting that the reduction may be produced by mechanical forces on the sensory nerve, rather than synaptically (Fig. 4). 4. The wind-response of interneurons is significantly diminished by the sensory reduction when measured either extra-or intracellularly (Figs. 5, 6). Cells affected include identified ventral and dorsal giant interneurons (GI's), which carry directional information about wind from the abdominal cerci to the more anterior portions of the nervous system, and are involved in flying (Camhi 1980; Ritzmann 1984; Comer 1985). 5. The reduction in the interneuronal response was unaffected by the elimination of input from descending central pathways, and input from a cercal chordotonal organ that senses cercal position and inhibits some of the GI's (Fig. 5). Thus, the reduction in wind-evoked sensory activity can itself account for the modulation of interneuron activity. 6. The extracellularly recorded response of the nerve cord to wind was divided into: large action potentials (AP's) that included almost all of the GI AP's (Fig. 6B), and smaller AP's of unidenti-Abbreviations: GI giant interneuron; AP action potential * To whom offprint requests should be sent fled cells. The activity of both small and large AP's is reduced by medial displacement of the cercus. However, the large AP's are significantly more reduced (Fig. 6). The small AP's comprise between one-half and two-thirds of the number of AP's recorded in response to wind. 7. The sensory reduction may serve to protect the circuitry of the exquisitely sensitive wind-sensitive escape system from habituation by the strong winds generated when the animal flies.
Journal of Neurobiology, 1990
The data described here complete the principal components of the cockroach wind-mediated escape circuit from cercal afferents to leg motor neurons. It was previously known that the cercal afferents excite ventral giant interneurons which then conduct information on wind stimuli to thoracic ganglia. The ventral giant interneurons connect to a large population of interneurons in the thoracic ganglia which, in turn, are capable of exciting motor neurons that control leg movements. Thoracic interneurons that receive constant short latency inputs from ventral giant interneurons have been referred to as type A thoracic interneurons (T1,s). In this paper, we demonstrate that the motor response of TIAs occurs in adjacent ganglia as well as in the ganglion of origin for the TIa. We then describe the pathway from T14s to motor neurons in both ganglia. Our observations reveal complex interactions between thoracic interneurons and leg motor neurons. Two parallel pathways exist. TIAs excite leg motor neurons directly and via local interneurons. Latency and amplitude of post-synaptic potentials (PSPs) in motor neurons and local interneurons either in the ganglion of origin or in adjacent ganglia are all similar. However, the sign of the responses recorded in local interneurons (LI) and motor neurons varies according to the TIA suhpopulation based on the location of their cell bodies. One group, the dorsal posterior group, (DPGs) has dorsal cell bodies, whereas the other group, the ventral median cells, (VMC) has ventral cell bodies. All DPG interneurons either excited postsynaptic cells or failed to show any connection a t all. In contrast, all VMC interneurons either inhibited postsynaptic cells or failed to show any connection. It appears that the TIas utilize directional wind information from the ventral giant interneurons to make a decision on the optimal direction of escape, The output connections, which project not only to cells within the ganglion of origin but also to adjacent ganglia and perhaps beyond, could allow this decision to be made throughout the thoracic ganglia as a single unit. However, nothing in these connections indicates a mechanism for making appropriate coordinated leg movements. Because each pair of legs plays a unique role in the turn, this coordination should be controlled by circuits dedicated to each leg. We suggest that this is accomplished by local interneurons between TIAS and leg motor neurons.
The Journal of Neuroscience, 2015
Stimulus-specific adaptation (SSA) is considered to be the neural underpinning of habituation to frequent stimuli and novelty detection. However, neither the cellular mechanism underlying SSA nor the link between SSA-like neuronal plasticity and behavioral modulation is well understood. The wind-detection system in crickets is one of the best models for investigating the neural basis of SSA. We found that crickets exhibit stimulus-direction-specific adaptation in wind-elicited avoidance behavior. Repetitive air currents inducing this behavioral adaptation reduced firings to the stimulus and the amplitude of excitatory synaptic potentials in wind-sensitive giant interneurons (GIs) related to the avoidance behavior. Injection of a Ca 2ϩ chelator into GIs diminished both the attenuation of firings and the synaptic depression induced by the repetitive stimulation, suggesting that adaptation of GIs induced by this stimulation results in Ca 2ϩ-mediated modulation of postsynaptic responses, including postsynaptic short-term depression. Some types of GIs showed specific adaptation to the direction of repetitive stimuli, resulting in an alteration of their directional tuning curves. The types of GIs for which directional tuning was altered displayed heterogeneous direction selectivity in their Ca 2ϩ dynamics that was restricted to a specific area of dendrites. In contrast, other types of GIs with constant directionality exhibited direction-independent global Ca 2ϩ elevation throughout the dendritic arbor. These results suggest that depression induced by local Ca 2ϩ accumulation at repetitively activated synapses of key neurons underlies direction-specific behavioral adaptation. This input-selective depression mediated by heterogeneous Ca 2ϩ dynamics could confer the ability to detect novelty at the earliest stages of sensory processing in crickets.
1987
1. 1. The campaniform sensilla on the wings of the locust are strain-sensitive mechanoreceptors that provide proprioceptive feedback about wing forces, particularly aerodynamic lift, experienced during flight. They can be excited by imposed deformations of the wing, including those caused by imposed wing twisting. The afferents of the single subcostal group of sensilla on the hindwing had the same directional selectivity for supinating twist and shared the properties of a dynamic sensitivity and adaptation. A group of strain-sensitive mechanoreceptors with similar properties, presumably campaniform sensilla, is also found in the forewings. 2. 2. Four types of thoracic interneurones influenced by these factors were recorded and stained intracellularly. The response of interneurone 5AA to imposed deformations of the hindwing ipsilateral to its soma is determined by excitatory chemical synaptic input from the campaniform sensilla. Interneurone and sensilla have a common directional sel...
Journal of Neurophysiology, 1991
1. Six different types of primary wind-sensitive interneurons in the cricket cercal sensory system were tested for their sensitivity to the orientation and peak velocity of unidirectional airflow stimuli. 2. The cells could be grouped into two distinct classes on the basis of their thresholds and static sensitivities to airflow velocity. 3. Four interneurons (the right and left 10–2 cells and the right and left 10–3 cells) made up one of the two distinct velocity sensitivity classes. The mean firing frequencies of these interneurons were proportional to the logarithm of peak stimulus velocity over the range from 0.02 to 2.0 cm/s. 4. The other two interneurons studied (left and right 9-3) had a higher air-current velocity threshold, near the saturation level of the 10–2 and 10–3 interneurons. The slope of the velocity sensitivity curve for the 9–3 interneurons was slightly greater than that for the 10–2 and 10–3 interneurons, extending the sensitivity range of the system as a whole t...