Buhl E et al. (2015), Sensory initiation of a co-ordinated motor resp...

XB-ART-50941

J Physiol 2015 Oct 01;59319:4423-37. doi: 10.1113/JP270792.

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Sensory initiation of a co-ordinated motor response: synaptic excitation underlying simple decision-making.

Buhl E , Soffe SR , Roberts A .

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Deciding whether or how to initiate a motor response to a stimulus can be surprisingly slow and the underlying processes are not well understood. The neuronal circuitry that allows frog tadpoles to swim in response to touch is well characterized and includes excitatory reticulospinal neurons that drive swim circuit neurons. Build-up of excitation to reticulospinal neurons is the key decision-making step for swimming. Asymmetry in this build-up between the two sides allows bilateral initiation at the same time as avoiding inappropriate co-activation of motor antagonists. Following stronger stimuli, reticulospinal neurons are excited through a trigeminal nucleus pathway and swimming starts first on the stimulated side. If this pathway fails or is lesioned, swimming starts later on the unstimulated side. The mechanisms underlying initiation of a simple tadpole motor response may share similarities with more complex decisions in other animals, including humans. Animals take time to make co-ordinated motor responses to a stimulus. How can sensory input initiate organized movements, activating all necessary elements at the same time as avoiding inappropriate co-excitation of antagonistic muscles? In vertebrates, this process usually results in the activation of reticulospinal pathways. Young Xenopus tadpoles can respond to head-skin touch by swimming, which may start on either side. We investigate how motor networks in the brain are organized, and whether asymmetries in touch sensory pathways avoid co-activation of antagonists at the same time as producing co-ordinated movements. We record from key reticulospinal neurons in the network controlling swimming. When the head skin is stimulated unilaterally, excitation builds up slowly and asymmetrically in these neurons such that those on both sides do not fire synchronously. This build-up of excitation to threshold is the key decision-making step and determines whether swimming will start, as well as on which side. In response to stronger stimuli, the stimulated side tends to 'win' because excitation from a shorter, trigeminal nucleus pathway becomes reliable and can initiate swimming earlier on the stimulated side. When this pathway fails or is lesioned, swimming starts later and on the unstimulated side. Stochasticity in the trigeminal nucleus pathway allows unpredictable turning behaviour to weaker stimuli, conferring potential survival benefits. We locate the longer, commissural sensory pathway carrying excitation to the unstimulated side and record from its neurons. These neurons fire to head-skin stimuli but excite reticulospinal neurons indirectly. We propose that asymmetries in the sensory pathways exciting brainstem reticulospinal neurons ensure alternating and co-ordinated swimming activity from the start.

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	Figure 1. Swimming in response to head‐skin stimulation A, tadpole and video frames (150 frames s–1) showing a tadpole viewed from above responding to touch on the left side of the head with a fine hair (arrow) by flexing to the left (frames 4–10) and then swimming off (frames 14–18). B, tracings from six similar videos after head stimulation on the left side (asterisk) plot head position to show flexion to left or right and swimming in a range of directions (arrows). C and D, an immobilized tadpole showing the brain, spinal cord and innervation of head skin by a sensory neuron in the trigeminal ganglion (tg). The positions of suction electrodes to record ventral root activity from swimming muscles (Rr, Rc, Lr, Lc) and to stimulate the right head skin are indicated. Fictive swimming can start on the stimulated side after touch (arrow, C) or current pulse (asterisk, D) stimulation to the head skin. E, histogram of latencies to the start of swimming in immobilized tadpoles following skin stimulation on the same (red bars) or opposite (black bars) side of the head. Bin size = 5 ms.
	Figure 2. Excitation and alternating firing of reticulospinal dINs on both sides after head‐skin stimulation A, positions of recording and stimulating electrodes. B, photograph of a recorded pair of dINs on either side of the hindbrain (dorsal view, rostral to the left; red rectangle in A) with soma, dendrites and both ascending and descending axons. The descending axon of the left side dIN was damaged during the dissection (at*). C and D, each panel shows three overlain responses from the right ventral root and the pair of dINs shown in B. In each case, swimming starts following a left head‐skin stimulus (at arrowhead) and grey bars show the phase when spikes occur on the unstimulated side. C, the first dIN spike is at short latency on the left, stimulated side (red). D, there is a short‐latency EPSP in the left dINs but the first spike is later on the unstimulated right side (black) and is followed by the first spike on the stimulated side.
	Figure 3. Alternating pattern of first and second reticulospinal dIN spike times on each side of the body following head‐skin stimulation A and B, responses from a pair of dINs different from the one shown in Fig. 2. In each case, activity starts following a head‐skin stimulus (at arrowhead) and grey bars show the phase when spikes occur on the unstimulated side. A, the first dIN spike is at short latency on the stimulated side (red), whereas, in B, the first spike is later on the unstimulated side (black) and each is followed by the first spike on the other side. C, plots show spike occurrences on each side at different times after a stimulus to one side of the head (red and pink bars are the stimulated side; black and grey are the unstimulated side). Measures are from 230 responses in six dIN pairs. Bin size = 5 ms.
	Figure 4. Asymmetry in EPSP responses to low‐level skin stimulation in dINs on stimulated (red) and unstimulated (black) sides A–C, example EPSPs in response to low level stimulation show differences between the two sides in recordings from three different dIN pairs. D, averages of 10 responses from records in C (continuous lines) show that the stimulated side EPSPs are earlier and rise faster. Dotted lines either side of curves are the SDs.
	Figure 5. Effects of removing the tIN population on one side on swimming responses to head‐skin stimulation A, stimulation and recording set‐up and area where tINs were removed (blue). B, side of first ventral root response (mean ± SD) to electrical stimulation and light dimming in control (black) and treated animals with tINs removed on the stimulated side (blue). Responses to light were similar before and after treatment. C, delays to first ventral root response (median, IQR) on the stimulated and unstimulated side following head‐skin stimulation. Delays increase significantly after removal of the tINs on the treated side only. Asterisks indicate a significant difference at P < 0.0001 (Mann–Whitney test).
	Figure 6. Lesion experiments showing where trigeminal excitation can cross to the unstimulated side in the caudal hindbrain A, summary of regions of the hindbrain where unilateral transection prevented swimming (pink) or where mid‐line cuts (green) still allowed the initiation of bilateral swimming following a head‐skin stimulus applied to the right side (rhombomeres numbered). The trigeminal ganglia on the left side were severed to prevent contralateral sensory access (red line). B, example of a rostral unilateral transection (pink line). C, ventral root recordings show this lesion prevented swim initiation to a head‐skin stimulus (arrowhead) but not to a trunk‐skin stimulus (D). E, example of a mid‐line lesion (green line) that only left a short intact region of caudal hindbrain (arrow). F, this short intact region was sufficient to allow initiation of bilateral swimming following a head‐skin stimulus to the right side. Ventral root recording positions on right (upper traces) and left (lower traces) sides are indicated in B and E.
	Figure 7. Sensory pathway rostral dorsolateral commissural neurons (rdlcs) respond to head and trunk skin stimulation A, dorsal view showing the position of the stimulating and recording electrodes. B, rdlc neurobiotin filling showing the extent of the axon in hindbrain, with enlarged tracing of rdlc with soma, dendrites and axon crossing the mid‐line and ascending and descending on the contralateral side. C and D, traces showing rdlc response to ipsilateral trunk and head‐skin stimulation (arrowhead) of increasing strength from black = no response, red = EPSP alone, blue = spike, green = response to strong stimulus. E, current injected into an rdlc evokes a single spike at threshold and fast multiple firing at higher levels. F, showing the position of the electrodes for paired recording and a record of responses of rdlc and dIN to right head stimulus that starts swimming, as well as low and higher magnification tracings of the recorded cells in the box. G, responses of another rdlc/dIN pair to head‐skin stimuli, aligned by rdlc spikes to show EPSPs with variable delays (arrowheads) and shapes. Coupling artefact indicated by an asterisk (*).
	Figure 8. Swim initiating network A, brain in dorsal view and the head‐skin trigeminal pathways initiating swimming on the same or opposite sides. Dots show locations of the neuron populations, not their real numbers: touch‐sensory trigeminal neurons (tSt, yellow), sensory pathway neurons (tIN, pale magenta; rdlc, red), electrically coupled reticulospinal excitatory neurons (dIN, brown). Fb, forebrain; hb, hindbrain; mb, midbrain; m, muscles; oc, otic capsule; sc, spinal cord; tg, trigeminal ganglion. B, functional diagram of the network including the central pattern generator (swim circuit) neurons: inhibitory interneurons (cIN, blue; aIN, purple) and motoneurons (mn, green). Continuous lines indicate evidence for a monosynaptic connection. Dashed lines indicate indirect connections (delay). Large circles represent populations of neurons. Small circles (inhibitory) and triangles (excitatory) are synapses and, when they contact a box, they connect to all neurons in the box.

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