Learning from the spinal cord: How the study of spinal cord plasticity informs our view of learning

Abstract

The paper reviews research examining whether and how training can induce a lasting change in spinal cord function. A framework for the study of learning, and some essential issues in experimental design, are discussed. A core element involves delayed assessment under common conditions. Research has shown that brain systems can induce a lasting (memory-like) alteration in spinal function. Neurons within the lower (lumbosacral) spinal cord can also adapt when isolated from the brain by means of a thoracic transection. Using traditional learning paradigms, evidence suggests that spinal neurons support habituation and sensitization as well as Pavlovian and instrumental conditioning. At a neurobiological level, spinal systems support phenomena (e.g., long-term potentiation), and involve mechanisms (e.g., NMDA mediated plasticity, protein synthesis) implicated in brain-dependent learning and memory. Spinal learning also induces modulatory effects that alter the capacity for learning. Uncontrollable/unpredictable stimulation disables the capacity for instrumental learning and this effect has been linked to the cytokine tumor necrosis factor (TNF). Predictable/controllable stimulation enables learning and counters the adverse effects of uncontrollable simulation through a process that depends upon brain-derived neurotrophic factor (BDNF). Finally, uncontrollable, but not controllable, nociceptive stimulation impairs recovery after a contusion injury. A process-oriented approach (neurofunctionalism) is outlined that encourages a broader view of learning phenomena.

Spinal mediation of motor learning and memory in the rat fetus

“…Because the transection was performed after an initial training session, but before the second training, the savings reported in Experiment 2 suggests that information acquired during normal yoke training is stored in the spinal cord, and that fetuses continue to have access to that information after connections with the brain have been severed. Taken together, these experimental results add to a growing number of examples illustrating the plasticity and learning capacity of the isolated spinal cord (Grau 2014; Grau et al, 2006; Wolpaw 2006, 2007). …”

“…Although spinal neural systems are often taken to be synonymous with reflexive, rigid or pre-programmed responses, there is a growing literature on the ability of the spinal cord to support learning, including habituation and sensitization, Pavlovian and instrumental conditioning (Grau, 2014; Grau, et al, 2006; Thompson & Spencer, 1966; Wolpaw, 2006, 2007). Various forms of locomotor training, such as stepping on a treadmill or with a robotic assistive device, are helpful in promoting recovery of locomotor function after spinal cord trauma (Edgerton & Roy, 2009; Raineteau & Schwab, 2001; see also Teulier, Lee & Ulrich, this issue).…”

Developmental plasticity of coordinated action patterns in the perinatal rat

“…For example, rats that underwent a mid-thoracic spinal transection shortly after birth showed the same developmental changes in motorneuron morphology seen during normal development, whereas rats that received the transection as weanlings or adults showed regressive changes in motorneuron morphology (Cummings & Stelzner, 1988). Although sparing of function is greatest in immature animals, the adult spinal cord retains some level of plasticity, as both classical and operant conditioning has been shown to occur in the adult cord (Crown, Ferguson, Joynes, & Grau, 2002; Grau, 2014; Wolpaw, 2006). …”

Spinal microcircuits comprising dI3 interneurons are necessary for motor functional recovery following spinal cord transection

“…Such changes have been proposed to underlie spontaneous or training-induced changes in motor output in spinal cord injury patients (Harkema, 2008; Knikou, 2010; Dietz, 2012) and in animal models of spinal cord injury (Côté and Gossard, 2004; Frigon et al, 2009; Tillakaratne et al, 2010; Martin, 2012; van den Brand et al, 2012; Houle and Côté, 2013; Takeoka et al, 2014). Similar mechanisms of plasticity may also occur during learning in intact developing and mature spinal cords (Tahayori and Koceja, 2012; Grau, 2014). Studying such changes at synapses between dI3 INs and their target locomotor circuit neurons may reveal specific mechanisms underlying this plasticity.…”

“…Like other regions of the central nervous system, the spinal cord is remarkably plastic (Wolpaw, 2007; Grau, 2014). Such plasticity has been demonstrated, for example, following spinal cord injury, when training can lead to a degree of recovery of spinal locomotor circuits such that stepping movements are restored (Barbeau et al, 1987; Courtine et al, 2009; Harkema et al, 2012; Hubli and Dietz, 2013; Martinez et al, 2013; Takeoka et al, 2014).…”