10/26/2011 Reading 1. Craspe, T. B. and Sommer, M. A. (2008). - PDF document

10/26/2011 Reading 1. Craspe, T. B. and Sommer, M. A. (2008). Corollary discharge across the animal kingdom. Nature Reviews Neuroscience 9, 587 ‐ 600. L35. Sensory ‐ Motor Integration The Corollary Discharge in the Animal 2. Poulet, J. F. A. (2005). Corollary discharge inhibition and audition in the stridulating cricket. J. Comp. g p Kingdom Kingdom Physiol. A. 191, 979 ‐ 986. October 26, 2011 3. Poulet, J. F. and Hedwig, B. (2006). The cellular basis C. D. Hopkins of a corollary discharge. Science 311, 518 ‐ 22. Sensory ‐ Motor Integration “Much of sensory processing involves the generation of expectations or predictions about sensory input, and subsequent removal of such expectations from the sensory inflow.” Bell, C (1997) Brain, Behavior, Evolution 50 (suppl.) 17-31. Drone fly, Eristalis igives an optomotor response to a moving striped drum. normal optomotor reversed optomotor Eristalis head turned 180 normal In response to any self ‐ movement, the normal fly ignores the stationary striped drum while a head ‐ reversed fly oscillates back and forth in response to self ‐ initiated movements. retina A above newt with normal retina, A, above retina B and C below newt with retina B and D (below) Sperry, R. W. (1956). The eye and the brain. Scientific American Holst E. von and Mittelstaedt H. (1950) Das Reafferenzprincip. Naturwissenschaften 37, 464 ‐ 476. 1

10/26/2011 Corollary Discharge and Efference Copy • Erich von Holst and Horst Mittlesteadt (1950) • Roger Sperry (1950) Konrad Lorenz Erich von Holst Erich von Holst , 1908-1962 Sperry, R. W. (1950). Neural basis of the Holst E. von and Mittelstaedt H. (1950) spontaneous optokinetic response produced Das Reafferenzprincip. by visual inversion. Journal of Comparative and Naturwissenschaften 37, 464 ‐ 476. Physiological Psychology 43:483 ‐ 489. Expected Sensory Input and the Reafference E. von Holst and H. Mittelstaedt Principle • • Principle: every motor act causes Move eyes or head. “The Reafference Principle: some sort of sensory response • interaction between the central Retinal image shifts that can be used by animal to nervous system and periphery” control subsequent actions. (1950). • Expected shift: things are • Sensory feedback from motor act normal. Higher brain center, Z has connections can be useful ‐‐ even vital ‐‐ to can be useful even vital to • for both motor output (efference) and ( ) Unexpected intput: the visual animal’s performance. sensory responses (afferences). world is shifting, take action. • Sensory feedback that differs When a ‘motor command’ arises from a from expected can be used to higher center, the afferent feedback is control subsequent action. called ‘reafference’. Simultaneous with the efference, there is a second, internal, efference copy (EK). Holst E. von and Mittelstaedt H. ( 1950 ) Compared to reafference, and appropriately delayed, it serves to tell Da;. Reafferenzprincip. whether sensory feedback is as Naturwissenschaften 37, 464 ‐ 476. 10 9 expected. Reafference Illustration of the Reafference Principle: a) Reafference circuit for the control of eye movements. Zn = higher visual center Z1 = lower visual center E = efference (output to muscles) A = reafference (visual motion) a) The immobilized eye receives a command to turn the eye to the right. The eye muscles are immobilized by curare: the efference copy is present in the lower center, Z1 (a negative image of the expected reafference). The visual world appears to move to the left. b) The object moves to the right; the image on the retina moves from 1 to 2 causing afference. c) The eye is passively moved to the right by exerting pressure on the eyeball. The image of object moves across retina. d) The command to move the eye to the right, causes the image to shift from 1 to 2, also causing afference, but now, it is expected. It is removed from the sensory stream in Z1. 11 12 2

10/26/2011 Using von Holst and Mittelstaedt’s terminology: Efference: output (motor) Afference: input (sensory) Exafference: sensory response to events in the environment. Reafference: sensory response resulting from animal’s own movements. Efference copy: a copy of the motor efference, sent to the sensory system. When efference copy is added to reafference, the result is zero. Any left over sensation must this one is be exafference. incorrect http://www.urllabs.com/wad/ia/corollar/corollar.htm Craspe, T. B. and Sommer, M. A. (2008). Corollary discharge across the animal kingdom. Nature Reviews Neuroscience 9, 587 ‐ 600. Craspe, T. B. and Sommer, M. A. (2008). Corollary discharge across the animal kingdom. Nature Reviews Neuroscience 9, 587 ‐ 600. Crayfish Escape Response Classification scheme for Corollary Discharges invertebrate examples only in vertebrates 3

10/26/2011 James Poulet and Berthold Hedwig: Corollary discharge maintains Cricket Stridulation auditory sensitivity during sound production in crickets. Cricket Gryllus bimaculatus Omega Neuron 1 (ON1) responds to continuous sounds except when stridulating silent singing; no sound production during fictive singing stimulus sounds ON1 receives inhibition during fictive singing (nerve roots between ganglia and Mesothoracic ganglion motor sense organs and muscles behavior are cut) mesothoracic ganglia stimulus sounds inhibition is from motor program, not from some other sensory feedback In response the silent singing (one wing), there are Primary Afferent What about the primary afferent neuron? Is the Depolarizations in synchrony with the moving wing (no sound). afferent nerve silent during singing? For silent singing afferent does not generate spikes as Record from auditory before. afferents near the terminals Note the primary N t th i on ON1. afferent Afferents respond in phase depolarizations with sound. Soft sounds (PAD). give primary afferent Timing of PADs is depolarizations (PAD) similar to timing of (arrow). IPSPs in ON1. 4

10/26/2011 The primary afferent from the ear is not silenced by these Even after removal of the ears, the PAD is present in the auditory PADs, nor is it excited. afferent. No inhibition or PAD during fictive excitation from PADs. singing Response to sound is normal during silent wing movements. even get PAD if ears are removed. Conclusion: primary afferent depolarizations are a type of pre- synaptic inhibition How effective is the inhibition of ON1 soft sounds evoke spikes (post synaptic and pre-synaptic) During silent singing, chirps loud, then soft, shows that loud sounds presented to cricket at cause ON1 to adapt, not respond to soft typical volume. sounds. Note decrement during hyperpolarize during loud prevents motor action. spiking, and prevents adaptation. Corollary Discharge Interneuron CDI Record from auditory neurons in Conclusion: prothoracic ganglion and from interneurons in mesothoracic (CPG for song). CDI: extensive projection throughout CNS In cricket, motor output is accompanied by a corollary discharge which interacts with primary acoustic afferents, and with Omega neuron 1. -- cell body and dendrites in Meso., can Both inputs inhibit the response to sound, reducing the response get input from CPG to the loud sound. t th l d d -- prothroracic dendrites overlap auditory inputs The overall effect is to prevent over-stimulation, thereby maintaining sensitivity. -- other terminals – interaction with other sensory inputs consequent on singing. Poulet, J. F . and Hedwig, B. (2006). The cellular basis of a corollary discharge. Science 311, 518-22. 5

10/26/2011 CDI during motor output CDI is not part of CPG PSTH corresponds to wing CDI fires during singing closure (sound phase) phase response, Q = duration of ongoing chirp period N/dur . chirp period N+1 CDI is CDI is inhibited during flight stimulated by song production unresponsive to sounds 6

10/26/2011 Conclusions Mormyrid electric fish produce an ‘electro-motor’ command, and receive a electrosensory response as a consequence. In the cricket, an efferent signal works at two levels in the auditory system Pre-synaptic inhibition by PAD's in the afferent auditory terminal Post-synaptic inhibition by IPSP's in ON1 The efferent signal is a corollary discharge because it is generated in the nervous system and it's strength is independent of sound production The corollary discharge corresponds closely in timing to sound production Corollary discharges effectively reduce desensitization 40 Knollenorgans blank inputs by inhibition --Primary afferent (blue) EOD command terminates on nELL cell (yellow) with ipsp in nELL cell --large calyx-like synapses (electrotonic). --fibers from EOD afferent command (eocd) command (eocd) EODc EODc produce spikes that arrive at same time that command EOD would be fired. --sharp inhibition IPSP blocks spike at the time when EOD is EOD expected -- removes expected EOD XU-FRIEDMAN, M. A. & HOPKINS, C. D., 1999.- J. Exp. Biol. , 202:1311-1318. 41 42 FRIEDMAN, M.A. & HOPKINS, C.D. 1998 – J. Neurosci.18:1171-1185. 7