Disruption and rescue of interareal theta phase coupling and adaptive behavior
Proceedings of the National Academy of Sciences, USA
Rescuing executive functions in people with neurological and neuropsychiatric disorders has been a major goal of psychology and neuroscience for decades. Innovative computer-training regimes for executive functions have made tremendous inroads, yet the positive effects of training have not always translated into improved cognitive functioning and often take many days to emerge. In the present study, we asked whether it was possible to immediately change components of executive function by directly manipulating neural activity using a new stimulation technology called high definition transcranial alternating current stimulation (HD-tACS). Twenty minutes of in-phase stimulation over medial frontal cortex (MFC) and right lateral prefrontal cortex (lPFC) synchronized theta (~6 Hz) rhythms between these regions in a frequency and spatially specific manner, and rapidly improved adaptive behavior with effects lasting longer than 40 minutes. In contrast, anti-phase stimulation in the same individuals desynchronized MFC-lPFC theta phase coupling and impaired adaptive behavior. Surprisingly, the exogenously driven impairments in performance could be instantly rescued by reversing the phase angle of alternating current. The results suggest that executive functions can be rapidly up- or down-regulated by modulating theta phase coupling of distant frontal cortical areas, and contribute to the development of new tools for potentially normalizing executive dysfunction in patient populations.
Using transcranial direct-current stimulation (tDCS) to understand cognitive processing
Attention, Perception, & Psychophysics
Reinhart RMG, Fukuda K, Cosman JD, Woodman GF
Noninvasive brain stimulation methods are becoming increasingly common tools in the kit of the cognitive scientist. In particular, transcranial direct-current stimulation (tDCS) is showing great promise as a tool to causally manipulate the brain and understand how information is processed. The popularity of this method of brain stimulation is based on the fact that it is safe, inexpensive, its effects are long lasting, and you can increase the likelihood that neurons will fire near one electrode and decrease the likelihood that neurons will fire near another. However, this method of manipulating the brain to draw causal inferences is not without complication. Because tDCS methods continue to be refined and are not yet standardized, there are reports in the literature that show some striking inconsistencies. Primary among the complications of the technique is that the tDCS method uses two or more electrodes to pass current and all of these electrodes will have effects on the tissue underneath them. In this tutorial, we will share what we have learned about using tDCS to manipulate how the brain perceives, attends, remembers, and responds to information from our environment. Our goal is to provide a starting point for new users of tDCS and spur discussion of the standardization of methods to enhance replicability.
Reinhart RMG, McClenahan L, Woodman GF
How do people get attention to operate at peak efficiency in high-pressure situations? We tested the hypothesis that the general mechanism that allows this is the maintenance of multiple target representations in working and long-term memory. We recorded subjects’ event-related potentials (ERPs) indexing the working memory and long-term memory representations used to control attention while performing visual search. We found that subjects used both types of memories to control attention when they performed the visual search task with a large reward at stake, or when they were cued to respond as fast as possible. However, under normal circumstances, one type of target memory was sufficient for slower task performance. The use of multiple types of memory representations appears to provide converging top-down control of attention, allowing people to step on the attentional accelerator in a variety of high-pressure situations.
Role of n-methyl d-aspartate receptors in action-based predictive coding deficits in schizophrenia
Kort NS, Ford JM, Roach BJ, Gunduz-Bruce H, Krystal JH, Jaeger J, Reinhart RMG, Mathalon DH
Background. Recent theoretical models of schizophrenia posit that dysfunction of the neural mechanisms subserving predictive coding contributes to symptoms and cognitive deficits, and this dysfunction is further posited to result from N-Methyl D-aspartate glutamate receptor (NMDAR) hypofunction. Previously, by examining auditory cortical responses to self-generated speech sounds, we demonstrated that predictive coding during vocalization is disrupted in schizophrenia. In order to test the hypothesized contribution of NMDAR hypofunction to this disruption, we examined the effects of the NMDAR antagonist, ketamine, on predictive coding during vocalization in healthy volunteers and compared them to the effects of schizophrenia. Methods. In two separate studies, the N1 component of the event-related potential (ERP) elicited by speech sounds during vocalization (Talk) and passive playback (Listen) were compared to assess the degree of N1 suppression during vocalization, a putative measure of auditory predictive coding. In the cross-over study, 31 healthy volunteers completed two randomly ordered test days, a saline day and a ketamine day. ERPs during the Talk/Listen task were obtained pre-infusion and during infusion on both days, and N1 amplitudes were compared across days. In the case-control study, N1 amplitudes from 34 schizophrenia patients and 33 healthy controls were compared. Results. N1 suppression to self-produced vocalizations was significantly and similarly diminished by ketamine (Cohen’s d=1.14) and schizophrenia (Cohen’s d=.85). Conclusions. Disruption of NMDARs causes dysfunction in predictive coding during vocalization in a manner similar to the dysfunction observed in schizophrenia patients, consistent with the theorized contribution of NMDAR hypofunction to predictive coding deficits in schizophrenia.
Electrical stimulation of visual cortex can immediately improve spatial vision
Reinhart RMG, Xiao W, McClenahan L, Woodman GF
We can improve human vision by correcting the optics of our lenses. However, after the eye transduces the light, visual cortex has its own limitations that are challenging to correct. Overcoming these limitations has typically involved innovative training regimes that improve vision across many days. In the present study, we wanted to determine whether it is possible to immediately improve the precision of spatial vision with noninvasive direct-current stimulation. Previous work suggested that visual processing could be modulated with such stimulation. However, the short duration and variability of such effects made it seem unlikely that spatial vision could be improved for more than several minutes. Here we show that visual acuity in the parafoveal belt can be immediately improved by delivering noninvasive direct current to visual cortex. Twenty minutes of anodal stimulation improved subjects’ vernier acuity by approximately 15% and increased the amplitude of the earliest visually evoked potentials in lockstep with the behavioral effects. When we reversed the orientation of the electric field, we impaired resolution and reduced the amplitude of visually evoked potentials. Next, we found that anodal stimulation improved acuity enough to be measurable with the relatively coarse Snellen test and that subjects with the poorest acuity benefited the most from stimulation. Finally, we found that stimulation-induced acuity improvements were accompanied by changes in contrast sensitivity at high spatial frequencies.