The spinobulbar system in lamprey

Abstract

Locomotor networks in the spinal cord are controlled by descending systems which in turn receive feedback signals from ascending systems about the state of the locomotor networks. In lamprey, the ascending system consists of spinobulbar neurons which convey spinal network signals to the two descending systems, the reticulospinal and vestibulospinal neurons. Previous studies showed that spinobulbar neurons consist of both ipsilaterally and contralaterally projecting cells distributed at all rostrocaudal levels of the spinal cord, though most numerous near the obex. The axons of spinobulbar neurons ascend in the ventrolateral spinal cord and brainstem to the caudal mesencephalon and within the dendritic arbors of reticulospinal and vestibulospinal neurons. Compared to mammals, the ascending system in lampreys is more direct, consisting of excitatory and inhibitory monosynaptic inputs from spinobulbar neurons to reticulospinal neurons. The spinobulbar neurons are rhythmically active during fictive locomotion, representing a wide range of timing relationships with nearby ventral root bursts including those in phase, out of phase, and active during burst transitions between opposite ventral roots. The spinobulbar neurons are not simply relay cells because they can have mutual synaptic interactions with their reticulospinal neuron targets and they can have synaptic outputs to other spinal neurons. Spinobulbar neurons not only receive locomotor inputs but also receive direct inputs from primary mechanosensory neurons. Due to the relative simplicity of the lamprey nervous system and motor control system, the spinobulbar neurons and their interactions with reticulospinal neurons may be advantageous for investigating the general organization of ascending systems in the vertebrate.

Figure 1

Similarity in the ascending inputs to uniquely identified reticulospinal neurons recorded in different animals. Intracellular recordings of membrane potential from three of the large uniquely identifiable Müller cells in the MRRN, B1, B3, and B4, in a split bath preparation in which the spinal cord was exposed to D-glutamate to induce locomotor activity and the brainstem bath was perfused with a high divalent cation solution to reduce polysynaptic pathways. The intracellular activity is referenced to the ipsilateral ventral root at spinal segment 10. The amplitudes and shapes of the ascending rhythmic inputs are similar in the two animals.

Figure 2

Examples of mutual interactions between descending reticulospinal neurons and ascending spinobulbar neurons. (A) Mutual excitation between a reticulospinal neuron in the PRRN and an ipsilateral excitatory SB neuron. (B) A Müller reticulospinal neuron that made a dual electrical – chemical excitatory synapse on an ipsilateral spinobulbar neuron was in turn inhibited by the same spinobulbar neuron. (Figure modified from Einum and Buchanan 2006).

Figure 3

Examples of the morphology of spinobulbar neurons injected with biocytin, reacted with horseradish peroxidase-avidin and drawn from wholemounts of the spinal cord. iSB = ipsilaterally-projecting spinobulbar neuron; bSB = bilaterally-projecting spinobulbar neuron; cSB = contralaterally-projecting spinobulbar neuron; a = axon. (Figure modified from Einum and Buchanan 2006).

Figure 4

Spinobulbar neurons not only have synaptic outputs in the brainstem but also within the spinal cord along both the ascending and descending axon branches. An example is shown of the output of a contralaterally-projecting spinobulbar neuron (cSB) that produced ipsps in unidentified neurons (UN) within the spinal cord both rostral and caudal to the soma of the cSB.

Figure 5

Rhythmic locomotor activity in spinobulbar neurons. (A) Paired recording of a motoneuron and an ipsilaterally-projecting spinobulbar neuron (iSB) in the same spinal segment during fictive swimming. The two cells had similar oscillatory envelopes and similar detailed synaptic activity. (B) Summary of timings of rhythmic activity in spinobulbar neurons. The phase of the peak depolarization of each cell is represented on a circular plot where 0.0 is the onset of the ipsilateral ventral root burst and 0.5 is the onset of the contralateral ventral root burst (B modified from Einum and Buchanan 2005).