Since the late nineteenth century, it has long been assumed that the language function is hierarchically organized into specific cortical areas, the Broca’s and Wernicke’s areas (1). However, over the past decades, several lines of evidence have shown that the language faculty not only engages a number of cortical and subcortical regions that extend far beyond the classical areas [for reviews, see for example (2, 3)] but it is also represented within regions that had never been considered before to support language [for review see Ref. (4)]. Accordingly, instead of considering the language faculty as completely modularized, behavioral and neuroimaging results have shown that the network subserving the language function is largely distributed across the brain (5, 6). In the embodied cognition view, the representation of a concept is crucially dependent upon the sensory–motor properties belonging to that concept (7–9). Indeed, the hypothesis has been advanced that action verbs are mentally represented in different semantic representations among which the sensorimotor features to perform the action (10–12). This implies that the sensory–motor regions of the brain may also process action concepts. Several lines of evidence have already suggested that the sensorimotor cortex takes part in language processing, at least when speech is translated into sensorimotor acts (10, 13, 14). Indeed, much of this evidence comes from studies that used action verbs (individually presented or embedded in sentences) as stimuli [e.g., Ref. (13, 15, 16)]. Accordingly, when people listen to verbal description of actions, their somatosensory, motor, and premotor neural populations are activated as they are actually performing the corresponding actions [5–3, for reviews see Ref. (4, 17)]. Recently, slower hand motor responses have been shown during processing of nouns referring to hand-related objects [(11, 12); see also Ref. (18)].

Thus, the retrieval of words associated with motor schemata, like swimming, is thought to rely in part in sensorimotor regions of the brain. Similarly, manipulable nouns (i.e., a pen), which recruit motor representations (i.e., writing), are partly processed in the same regions (11, 12).

Together with this more interactive view of language processing, the traditional concept of the spinal cord as a hardwired system that automatically respond to motor commands from the brain and to sensory inputs from the periphery has changed over time. Indeed, a large body of evidence has shown that this structure not only produces a variety of specialized movements but also acquires and memorizes new behaviors [see Ref. (19) for review].

However, in spite of a remarkable energy in considering the spinal cord as an active system which possesses capacities for neuronal and synaptic plasticity for the recovery of chronic pain and motor deficits (20, 21), as far as we know, no studies have considered whether it might also contribute as an auxiliary support for language processing.

Actually, although some earlier studies on acute traumatic spinal cord injury (SCI) patients have documented the presence of cognitive deficits in different domains, such as attention, executive functioning, memory, and language (22–27), none of them reported sufficient evidence that the cognitive impairment was specifically related to SCI. Indeed, factors contributing to those deficits were varied. Some patients had concomitant traumatic brain injury at the time of their accidents (26). Others had a history of cerebral vascular insufficiency (27). In addition, the long-term cognitive effects of alcohol and substance abuse, which have been found to approach a prevalence of 50% in the SCI population, may have contributed to cognitive or behavioral disorders (24, 25).

Given the wide variability of cortical lesions among aphasic patients, it is not always easy to localize through non-invasive brain stimulation techniques, such as transcranial direct current stimulation (tDCS), the optimal stimulation cortical sites, unless we use additional very expensive methodologies, such as neuroimaging and/or modeling (28, 29). This points to the urgency of considering other vicarious systems, functionally connected to the brain, that, when stimulated, contribute to the recovery of language.

Indeed, it has been shown that the application of tDCS over the motor cortex influences brain excitability, and hence can also modulate the spinal cord (30–32). By developing a constant low-intensity current (1–2 mA) through two large electrodes located on the targeted areas, tDCS increases or reduces cortical excitability after anodal or cathodal stimulation, respectively, possibly by inducing depolarization or hyperpolarization of the neuronal membrane resting potential (33–36). Accordingly, in a series of experiments performed in healthy subjects, Roche et al. (37, 38) showed that anodal tDCS over the motor cortex modified spinal network excitability by increasing disynaptic inhibition of spinal motoneurons. The authors suggested that the increase of disynaptic inhibition relies on an increase of disynaptic interneuron excitability and that tDCS over the motor cortex in human subjects induces effects on the spinal network. Similarly, Di Lazzaro et al. (39) found that 20 min of anodal tDCS over the primary motor cortex lead to a pronounced increase of D wave. Since the D wave is produced by direct activation of corticospinal axons (39), the authors concluded that anodal tDCS induced changes in excitability in corticospinal projections. Indeed, in patients with SCI, spinal plasticity induced by anodal tDCS over the motor cortex may promote the effects of locomotor training through modulation of spinal interneurons (32). On the other hand, it has also been shown that spinal manipulation, in stroke patients who are recovering from muscle degrading dysfunctions, leads to changes in cortical excitability, as measured by significant larger movement related cortical potential amplitudes after the treatment (40).

Therefore, given this strong reciprocal connections between the cortex and the spinal cord, we might assume that the stimulation of the spinal cord could influence activity into the sensorimotor cortex, through the ascending spinal pathways, which, in turn, might facilitate language processing (4, 16–18, 41).

To our knowledge, the impact of transcutaneous spinal direct current stimulation (tsDCS) on language recovery has not been investigated so far. A number of studies have already used tsDCS for modulating spinal cord activity in humans along the lemniscal pathway and nociceptive spinal system [(42–44), see Ref. (45) for review]. In most of these studies, the active electrode was placed over the thoracic vertebrae (T10–T12) and the reference electrode above the right arm while the current (2–3 mA) was delivered for 20–30 min (42–44, 46). Different from tDCS studies in which the anode applied over the cortical areas increases cortical excitability (30, 39, 47), in those works, anodal tsDCS had an overall inhibitory effect on spinal cord activity, while cathodal tsDCS did not produce polarity-specific effects (42, 43, 48). Interestingly for our study, it has also been shown that anodal tsDCS might elicit neurophysiological changes into the brain, through the activation of tonic afferent systems to the cortex (46–49). Indeed, Bocci et al. (46) assessed changes in intracortical excitability in 10 healthy subjects following tsDCS (2 mA, 20 min) over the thoracic vertebrae (T9–T11 level) by evaluating changes in motor-evoked potentials (MEPs) recorded from the first digital interosseus and the tibialis anterior muscles. Results showed that tsDCS was able to modulate intracortical excitability in a polarity-specific manner. Anodal tsDCS decreased MEP amplitudes, while cathodal tsDCS elicited opposite effects. Similarly, the same authors found that anodal tsDCS (T9–T11 level, 2 mA, 20 min) increased transcallosal conduction time and interhemispheric delay in motor connectivity, leading to a functional disconnection between hemispheres (49).

Therefore, given that one of the main function of the spinal cord is to translate sensory information into motor output and that tsDCS exerts its influence also into the brain (46–49), it is possible that tsDCS contributes to the recovery of language, in particular for those words characterized by motor properties, such as action verbs (i.e., to bite). Conversely, nouns not typically related to specific action (i.e., the cloud) would not activate the motor pathways and, therefore, should not benefit of this facilitation (11, 12).

In the present study, 14 aphasic participants underwent a daily language treatment for their word retrieval difficulties while delivering tsDCS. To ensure that the effects were specific for spinal cord stimulation and, therefore, that we were acting as far as possible from the cortex, we chose to stimulate the thoracic level. Based on previous results (11, 12), we expected to find a beneficial effect on response accuracy and vocal reaction times only for verbs.

This study assessed whether tsDCS coupled with language treatment improves word retrieval in persons with chronic non-fluent aphasia. Our findings showed that anodal tsDCS differently affected the amount of improvement in noun and verb naming. Indeed, while noun and verb naming significantly improved in all patients for each condition at the end of training due to language treatment, anodal tsDCS boosted recovery only for verbs. Moreover, FU testing showed that these effects lasted over 1 week after the intervention. This specificity argues against an effect simply due to enhanced cognitive arousal which should have influenced both verb and noun naming.

Although this finding seems surprising, it suggests that the spinal cord takes part in verb processing acting as a “bridge” for conveying tsDCS induced changes into brain networks. Thereby inducing neuromodulation effects into brain areas involved in verb naming.

As previously stated, opposite excitability changes induced by cortical tDCS (60, 61) and spinal tDCS (42, 44) of the same polarity have been reported. Indeed, while anodal tDCS is generally facilitatory to the cortex (30, 39, 47), anodal tsDCS was found to decrease the amplitude of the somatosensory evoked potentials (42), laser evoked potentials (44) and motor responses evoked by transcranial magnetic stimulation (46) due to an hyperpolarization of the axons running along the spinal columns, while cathodal stimulation did not exert any influence (42, 46). It has also been shown that thoracic tsDCS elicits intracortical changes through the thalamus and the reticular systems (46, 49). Indeed, recent modeling studies have proved that, despite some inter-individual differences, the electric field induced by thoracic tsDCS is longitudinally directed along the vertebral column, especially when the return electrode is placed over the right arm (62, 63). Yet, the electric field induced by thoracic tsDCS is maximum at thoracic level and it can increase the somatosensory activity from the spinal cord to the brain (62, 63).

Even if the exact underlying tsDCS mechanisms over the corticospinal system, in our study, remain largely speculative, the hypothesis might be advanced that anodal tsDCS has inhibited the tonic ascending system to the cortex, ultimately decreasing the activity into the sensorimotor areas. Paradoxically, the resulting reduction could have potentiated their function. Indeed, the hypothesis has been advanced that inhibitory current might decrease the excitability of cortical inhibitory interneurons (64, 65), thus improving the efficacy of their related areas. Following previous suggestion, we might also hypothesize that anodal tsDCS has increased the interhemispheric delay in motor connectivity (49), thus, enhancing the functionality of the left sensorimotor cortices through inhibition of its right homologs (66). Indeed, the model of interhemispheric competition between the residual language areas in the left-damaged hemisphere and the intact right hemisphere (akin to models of motor recovery after stroke) proposes that in patients with left hemispheric damage, the homotopic contralateral right hemispheric areas may be in a state of abnormally high activation and may exert an inhibitory effect over the damaged hemisphere (67, 68). Thus, improvement may be possible either by increasing the output of the perilesional left hemisphere through excitatory stimulation (59, 69–71) or decreasing the inhibition from the intact right hemisphere by applying inhibitory current over the contralesional cortex (72–75). Therefore, in our study, we might hypothesize that tsDCS has inhibited the right hemisphere areas increasing the left hemisphere activity and, in particular, the left sensorimotor areas, making them more efficient. Indeed, all patients had preserved motor cortex and the amount of improvement obtained for verbs in the anodal condition was similar across patients with a partial damage over the somatosensory areas (see Table 1) and the rest of the group [five damaged subjects: mean = 49% (SD = 12) p < 0.001 vs. nine undamaged subjects: mean = 38% (SD = 11) p < 0.001; difference between the two groups: mean = 11%, unpaired t-test p = 0.14].

An effect of tsDCS on pharmacologically defined systems cannot also be ruled out. Indeed, it has been shown that the mechanisms of action underlying tDCS could also involve receptors and neurotransmitters. For instance, neurotransmitters such as GABA and glutamate undergo substantial changes into the brain after cortical tDCS over the motor cortex (47, 76). Accordingly, Stagg et al. (76) found that excitatory (anodal) tDCS reduced GABA levels within the sensorimotor cortices while inhibitory (cathodal) stimulation reduced glutamatergic neuronal activity with a highly correlated reduction in GABA over the same region, due to the close biochemical relationship between the two neurotransmitters. A local decrease of GABA levels in the sensorimotor cortex is strongly related with synaptic plasticity and it is positively correlated with an improvement in motor learning (77–79). Although this effect might be task specific, one further hypothesis to consider is that, in our study, the inhibitory current delivered through anodal tsDCS has decreased both glutamate and GABA levels into the sensorimotor cortices leading to an improvement of their function (76, 78, 79).

All of the above mentioned hypotheses explain the specificity of anodal tDCS for verbs. As stated in the Introduction, several lines of evidence have already shown that action words are partly represented into the sensorimotor cortex due to their sensorimotor semantic properties which, in turn, are involved in action understanding and naming (4, 10–13, 15–18, 41). This implies that the sensorimotor cortex may also process action concepts (6). Yet, Repetto et al. (80) found that processing hand-related action words, but not abstract words, was impaired after repetitive TMS to the left primary motor cortex [see also Ref. (81)]. Similarly, very recently, Meinzer et al. (82) have shown that anodal tDCS delivered over the left motor cortex with concomitant language training improved naming abilities in a group of 26 patients with chronic aphasia.

Thus, we hypothesize that anodal tDCS has influenced neural activity along the ascending spinal pathways, ultimately modulating activity in the sensory–motor cortex. This has, in turn, facilitated verb retrieval. Indeed, the improvement found in verb naming was not specific for any type of action. Yet, the current delivered over the thoracic vertebrae going up to the brain also resulted in an improvement on verbs (i.e., hand and mouth actions) whose corresponding muscles are innervated above the stimulated region. This last result further confirms our hypothesis that action verbs were ultimately processed by the sensorimotor areas. On the contrary, since nouns do not express a motor content they did not benefit from stimulation.

In conclusion, although other studies will further elucidate our understanding on the role of the spinal cord in language processing, we believe that our results are promising since, for the first time, they suggest that spinal tDCS significantly affects the sensorimotor system removing the need to establish which part of this system should be targeted with tDCS. Since verbs play a crucial role in sentence construction which is essential to enhance speech production in persons with aphasia, we believe that this finding is important for treatment outcomes.

This study was carried out in accordance with the recommendations of the Helsinki Declaration and the Institutional Review Board of the IRCCS Fondazione Santa Lucia, Rome, Italy with written informed consent from all subjects. All subjects gave written informed consent in accordance with the Declaration of Helsinki. The protocol was approved by the Institutional Review Board of the IRCCS Fondazione Santa Lucia, Rome, Italy.

Conceived and designed the experiment: PM, VF, and AP. Performed the experiment: VF and JS. Analyzed the data: VF, TG, and GC. Wrote the paper: PM. Edited the manuscript: PM, CC, and AP.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.