State-dependent modulation of sensory feedback

Abstract

By tradition - and for historical reasons - reflex pathways and interneurones have been named by their dominating sensory input. Later studies have demonstrated that each individual interneurone, as a rule, receives a broad convergence from a large variety of sensory modalities, as well as inputs from one or more descending tracts. It is thus possible that the traditional nomenclature inadvertently has served as a 'straightjacket' for conceptual development in this field. Indeed, there is now much evidence in favour of the view that the many classes of spinal interneurones may be seen as 'functional units' representing different levels of muscle synergies, parts of movements, or even more integrated motor behaviour. Such 'functional units' may be used by (different) descending pathways to mediate the motor commands from the brain and integrate the appropriate (multimodal) sensory feedback into the central command. A given sensory stimulus would then be able to affect the motor output through a number of parallel, or alternative, segmental pathways belonging to different 'functional units'. If this were correct it would indeed be predicted, rather than coming as a surprise, that a given sensory stimulus can result in different outputs - even with a different sign - depending on the preceding selection of active 'functional units', i.e. the type of motor activity initiated by the brain.

Figure 1. Convergence on interneurones in the pathway of reciprocal Ia inhibition (A-C) and on interneurones in the Ib inhibitory pathway (D -F)

Circuit diagrams in A and D summarise several of the connections to these two types of interneurones. Recordings from a knee flexor motoneurone (B) demonstrate the spatial facilitation on combined stimulation of quadriceps (Q) Ia afferents and Deiters' nucleus (ND). The right-most records show the reduction of the IPSP when conditioned by the L5 + L6 ventral roots (recurrent inhibition, cf. circuit diagram in A). Direct recording from a Ia inhibitory interneurone (C) demonstrates the monosynaptic excitation from Q and ND and the disynaptic recurrent inhibition following stimulation of the L5 + L6 ventral roots. Recordings in E demonstrate the facilitatory interaction between a conditioning rubrospinal volley (NR) and a group I volley from Q. Note that the facilitation is only seen when the quadriceps volley is strong enough to activate Ib afferents (stimulation strength of 1.52 × threshold (T) for recruiting the most excitable nerve fibres). Recordings in F demonstrate the facilitatory interaction between cutaneous fibres (superficial peroneal nerve, SP) and group I afferents from the nerve to the plantaris muscle (Pl). Upper traces are intracellular records (voltage calibrations apply to these traces), while lower traces are incoming volleys recorded from the dorsal root entry zone. (B adapted from Hultborn & Udo, 1972; C from Hultborn et al. 1976; E from Hongo et al. 1969; F from Lundberg et al. 1977.)

Figure 2. Differential release of transmission in excitatory and inhibitory ‘flexor reflex afferents’ by brainstem lesions and spinal transection

The graph in A shows the time course of the effects of single conditioning volleys in the nerve to flexor digitorum longus (40 T) on monosynaptic reflexes evoked from knee flexor posterior-biceps and semitendinousus. In B the effects of pinching the heel was tested under similar conditions. C, diagram showing alternative reflex pathways from flexor reflex afferents (FRA) with descending excitatory connections to interneurones of these pathways and its inhibitory interactive connections with the other reflex pathways from FRA. (A and B adapted from Holmqvist & Lundberg, 1961; C adapted from Lundberg, 1973.)

Figure 3. Emergence of group I EPSPs in two gastrocnemius motoneurones following administration of l-DOPA (A) and during MLR-induced fictive locomotion (B and C)

A, upper panel, superimposed traces are averaged intracellular records whereas the lower trace shows a sample of the cord dorsum potentials. The intracellular traces show the response to a train of stimuli of the plantaris nerve (Pl; 1.4 T) before, 17 and 30 min after injection of l-DOPA. B, upper traces, superimposition of averaged responses to the group I stimulation, obtained before, during and after the locomotor period. The lowermost trace is the cord dorsum potential aligned with the averaged intracellular responses. C, top to bottom: (1) high gain intracellular responses in a gastrocnemius-soleus motoneurone to group I stimulation of the plantaris nerve tilted vertically (GS mn). These are expended periods (100 ms) obtained from (2) the slow low gain intracellular record displaying the locomotor drive potentials (E_m), and the electroneurograms from (3) the gastrocnemius-soleus nerves (GS) and (4) the tibialis anterior nerve (TA). The periods of the slow time base recordings, which are expanded in the upper vertical traces, are indicated by markers above the continuous recording. The group I stimulation coincides with the beginning of the fast vertical traces (as indicated in B). The beginning and the end of a period of continuous MLR stimulation are indicated at the bottom. (Modified from Gossard et al. 1994.)

Figure 4. Sensory control of spinal ‘functional units’ during different types of movements controlled from the brain (A) and ‘gating’ of reflex transmission during movement (B)

A, diagram illustrating spinal ‘functional units’ (in different colours) relating various muscle synergies, part of movements or more integrated motor behaviour. The diagram illustrates the idea that the brain is activating and mediating its effects through these ‘functional units’. The same interneurones are probably involved in several ‘functional units’, and these units should therefore be spatially overlapping. The drawing also illustrates that the sensory feedback is channelled through the ‘functional unit’ activated by the brain, as illustrated in more detail in Fig. 3C. B, diagram illustrating the phasic gating of reflex transmission during different phases of a movement (e.g. during locomotion).