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Berthold Hedwig

Publications and source records attributed to Berthold Hedwig.

8 recordsLinked to original sources

New insights into corollary discharges mediated by identified neural pathways.

Sensory systems respond not only to stimuli from the environment but also to cues generated by an animal's own behaviour. This leads to problems of sensory processing because self-generated information can occur at the same time as external sensory information. However, in motor regions of the CNS corollary discharges are generated during behaviour. These signals are not used to generate movements directly but, instead, interact with the processing of self-generated sensory signals. Corollary discharges transiently modulate self-generated sensory responses and can prevent self-induced desensitization or help distinguish between self-generated and externally generated sensory information. Here, we review recent work that has identified corollary discharge pathways at different levels of the CNS in vertebrates and invertebrates.

Action Potentials↗

Pulses, patterns and paths: neurobiology of acoustic behaviour in crickets.

Crickets use acoustic communication for pair formation. Males sing with rhythmical movements of their wings and the mute females approach the singing males by phonotaxis. Females walking on a trackball rapidly steer towards single sound pulses when exposed to split-song paradigms. Their walking path emerges from consecutive reactive steering responses, which show no temporal selectivity. Temporal pattern recognition is tuned to the species-specific syllable rate and gradually changes the gain of auditory steering. If pattern recognition is based on instantaneous discharge rate coding, then the tuning to the species-specific song pattern may already be present at the level of thoracic interneurons. During the processing of song patterns, changes in cytosolic Ca(2+ )concentrations occur in phase with the chirp rhythm in the local auditory interneurone. Male singing behaviour is controlled by command neurons descending from the brain. The neuropil controlling singing behaviour is located in the anterior protocerebrum next to the mushroom bodies. Singing behaviour is released by injection of cholinergic agonists and inhibited by gamma-butyric acid (GABA). During singing, the sensitivity of the peripheral auditory system remains unchanged but a corollary discharge inhibits auditory processing in afferents and interneurons within the prothoracic auditory neuropil and prevents the auditory neurons from desensitisation.

Animals↗

The cellular basis of a corollary discharge.

How do animals discriminate self-generated from external stimuli during behavior and prevent desensitization of their sensory pathways? A fundamental concept in neuroscience states that neural signals, termed corollary discharges or efference copies, are forwarded from motor to sensory areas. Neurons mediating these signals have proved difficult to identify. We show that a single, multisegmental interneuron is responsible for the pre- and postsynaptic inhibition of auditory neurons in singing crickets (Gryllus bimaculatus). Therefore, this neuron represents a corollary discharge interneuron that provides a neuronal basis for the central control of sensory responses.

Acoustic Stimulation↗

Auditory orientation in crickets: pattern recognition controls reactive steering.

Many groups of insects are specialists in exploiting sensory cues to locate food resources or conspecifics. To achieve orientation, bees and ants analyze the polarization pattern of the sky, male moths orient along the females' odor plume, and cicadas, grasshoppers, and crickets use acoustic signals to locate singing conspecifics. In comparison with olfactory and visual orientation, where learning is involved, auditory processing underlying orientation in insects appears to be more hardwired and genetically determined. In each of these examples, however, orientation requires a recognition process identifying the crucial sensory pattern to interact with a localization process directing the animal's locomotor activity. Here, we characterize this interaction. Using a sensitive trackball system, we show that, during cricket auditory behavior, the recognition process that is tuned toward the species-specific song pattern controls the amplitude of auditory evoked steering responses. Females perform small reactive steering movements toward any sound patterns. Hearing the male's calling song increases the gain of auditory steering within 2-5 s, and the animals even steer toward nonattractive sound patterns inserted into the species-specific pattern. This gain control mechanism in the auditory-to-motor pathway allows crickets to pursue species-specific sound patterns temporarily corrupted by environmental factors and may reflect the organization of recognition and localization networks in insects.

Acoustic Stimulation↗

Complex auditory behaviour emerges from simple reactive steering.

The recognition and localization of sound signals is fundamental to acoustic communication. Complex neural mechanisms are thought to underlie the processing of species-specific sound patterns even in animals with simple auditory pathways. In female crickets, which orient towards the male's calling song, current models propose pattern recognition mechanisms based on the temporal structure of the song. Furthermore, it is thought that localization is achieved by comparing the output of the left and right recognition networks, which then directs the female to the pattern that most closely resembles the species-specific song. Here we show, using a highly sensitive method for measuring the movements of female crickets, that when walking and flying each sound pulse of the communication signal releases a rapid steering response. Thus auditory orientation emerges from reactive motor responses to individual sound pulses. Although the reactive motor responses are not based on the song structure, a pattern recognition process may modulate the gain of the responses on a longer timescale. These findings are relevant to concepts of insect auditory behaviour and to the development of biologically inspired robots performing cricket-like auditory orientation.

Acoustic Stimulation↗

Corollary discharge inhibition of ascending auditory neurons in the stridulating cricket.

Acoustically communicating animals are able to process external acoustic stimuli despite generating intense sounds during vocalization. We have examined how the crickets' ascending auditory pathway copes with self-generated, intense auditory signals (chirps) during singing (stridulation). We made intracellular recordings from two identified ascending auditory interneurons, ascending neuron 1 (AN1) and ascending neuron 2 (AN2), during pharmacologically elicited sonorous (two-winged), silent (one-winged), and fictive (isolated CNS) stridulation. During sonorous chirps, AN1 responded with bursts of spikes, whereas AN2 was inhibited and rarely spiked. Low-amplitude hyperpolarizing potentials were recorded in AN1 and AN2 during silent chirps. The potentials were also present during fictive chirps. Therefore, they were the result of a centrally generated corollary discharge from the stridulatory motor network. The spiking response of AN1 and AN2 to acoustic stimuli was inhibited during silent and fictive chirps. The maximum period of inhibition occurred in phase with the maximum spiking response to self-generated sound in a sonorously stridulating cricket. In some experiments (30%) depolarizing potentials were recorded during silent chirps. Reafferent feedback elicited by wing movement was probably responsible for the depolarizing potentials. In addition, two other sources of inhibition were present in AN1: (1) IPSPs were elicited by stimulation with 12.5 kHz stimuli and (2) a long-lasting hyperpolarization followed spiking responses to 4.5 kHz stimuli. The hyperpolarization desensitized the response of AN1 to subsequent quieter stimuli. Therefore, the corollary discharge will reduce desensitization by suppressing the response of AN1 to self-generated sounds.

Acoustic Stimulation↗

A corollary discharge maintains auditory sensitivity during sound production.

Speaking and singing present the auditory system of the caller with two fundamental problems: discriminating between self-generated and external auditory signals and preventing desensitization. In humans and many other vertebrates, auditory neurons in the brain are inhibited during vocalization but little is known about the nature of the inhibition. Here we show, using intracellular recordings of auditory neurons in the singing cricket, that presynaptic inhibition of auditory afferents and postsynaptic inhibition of an identified auditory interneuron occur in phase with the song pattern. Presynaptic and postsynaptic inhibition persist in a fictively singing, isolated cricket central nervous system and are therefore the result of a corollary discharge from the singing motor network. Mimicking inhibition in the interneuron by injecting hyperpolarizing current suppresses its spiking response to a 100-dB sound pressure level (SPL) acoustic stimulus and maintains its response to subsequent, quieter stimuli. Inhibition by the corollary discharge reduces the neural response to self-generated sound and protects the cricket's auditory pathway from self-induced desensitization.

Acoustic Stimulation↗

Contralateral inhibition as a sensory bias: the neural basis for a female preference in a synchronously calling bushcricket, Mecopoda elongata.

Imperfect synchrony between male calls occurs widely in acoustically courting crickets and bushcrickets. Males which are able to establish the temporal leadership usually attract more females in choice experiments but the proximate mechanism for this precedence effect is unknown. Here we show that contralateral inhibition, the neural basis for lateral contrast enhancement in the auditory pathways of insects and vertebrates, is also the probable proximate neural mechanism for this female preference. We recorded simultaneously from a pair of identified auditory interneurons in the synchronizing bushcricket Mecopoda elongata. When two identical acoustic stimuli are presented from opposite directions, one preceding the other by 120 ms, the neural representation within the receiver is far stronger for the leader signal. This results from a suppression of the neural response to the follower chirp by reciprocal contralateral inhibition. The advantage of the representation of the leader is 2-3-fold with time delays between 70 and 130 ms; the most clear-cut female preferences have also been found with such delays in previous behavioural experiments. In time-intensity trading experiments, a lead by 120 ms could only be compensated for by increasing the amplitude of the follower signal by 7-11 dB. We discuss contralateral inhibition in auditory systems as a sensory bias that results in female preference for leading signals, with important evolutionary consequences for male calling strategies.

Acoustic Stimulation↗