Modularity in the intact and spinal cat: methods, issues and questions for the future

The paper by Etienne Desrochers and colleagues from the Frigon lab, published in the current issue of The Journal of Physiology (Desrochers et al. 2019), is an important contribution. They provide a clear demonstration of a synergy organization in the spinal cord of the cat that is closely similar before and after spinal transection, using the methods of Krouchev and colleagues (2006) of direct component analysis (DCA). This paper demonstrates unequivocally the level of organization of locomotor synergies defined in this way in the cat spinal cord and their robustness over variable conditions, including split belt manipulations. The correspondence of these spinal synergies in broad terms to intact synergies is made clear. Though this type of spinal synergy construction is already known in lower vertebrates (e.g. Kargo & Giszter, 2008), the quality and depth of analysis here and the application to locomotion in a large mammal model is an important and influential result. The data and analysis are excellent demonstrations of spinal synergy structures conserved after spinal cord injury (SCI). Testing over variations in conditions to demonstrate robustness of synergy is a critical feature of the data provided in the work of Desrochers et al. 2019. Beyond pattern generation, it now appears that modularity of pattern construction is also likely to be fundamental, and robust to perturbations.

What remains to be understood, and how do these data relate to prior studies? The DCA techniques focus specifically on burst onset and offset data. The method thus illuminates synchrony of drives at these time points. It suggests synchronous drives as the units of composition, consistent with the spatial synergy perspective. However, the important caveat needs to be made that these data and methods do not comment on the subsequent muscle balance in the synergy, but only on the muscle membership and covariation at onset and offset. They favour synchronous spatial synergies, but do not establish this in the same way as other methods such as Non‐negative matrix factorization (NNMF) or Independent Component Analysis (ICA) (Tresch et al. 2006). Based only on the DCA results, it remains conceivable that between onset and offset muscle balance in the synergy unit might vary, or that different multi‐peak activity might sometimes occur in some muscles between the clearly defined onset and offset events, for example in the more sophisticated intact cat motor patterns. The issue is whether in sophisticated locomotion the intact cat might sometimes form time‐varying synergies between these two events. Although this is perhaps unlikely, based on other work (Kargo & Giszter, 2008), it is important to consider the possibility until shown otherwise. It has been proposed in the literature that time‐varying units of composition might be organized at higher levels of the CNS and then imposed on the spinal organization for better pattern fitting to motor actions (see Giszter, 2015). While this is a remaining question, it is beyond the current data and analyses of Desrochers and colleagues, and does not detract from either the impact or importance of their seminal study. Nonetheless, it is important the reader realizes that the same membership, onset and offset are potentially also consistent with variations in muscle activation balance within the synergy through time, between the anchors provided by these initial and terminal coincidence conditions. As stated above, this might be a source of variation in intact versus spinal cats or across biomechanical conditions of locomotion under the influence of descending pathways in the intact cat. Different analyses (e.g. Tresch et al. 2006) might help address this question more precisely. In the same vein, clearly the intact cat has significantly more sophistication in the use of the hindlimbs than the simpler spinal cat locomotor production, and how this sophistication is elaborated beyond the tests of stable locomotion here is also a topic for speculation and future experiment. It would also be of great interest to understand how the adult motor patterns described here (in both intact and spinal cats) relate to the early motor production in kittens near birth and kittens spinalized at birth, in order to understand if the synergy structures shown here are determined early in life or are developmentally constructed and plastic in early motor development.

In summary, Desrochers and colleagues (2019) have established a very important set of results, and thereby they have also made more acute the need for fuller answers as to their neural bases, how spinal synergies are first constructed, how they are modified through development, if and how they are used in motor skill construction, and when and how a mammal instead abandons them and strikes out with completely novel muscle compositions. These issues are crucial for application of modularity analyses systematically in neurological disorders such as SCI. Desrochers et al. have added a critical piece to the puzzle.