Does mismatch negativity have utility for NMDA receptor drug development in depression?

Nicholas Murphy, Marijn Lijffijt, Nithya Ramakrishnan, Bylinda Vo-Le, Brittany Vo-Le, Sidra Iqbal, Tabish Iqbal, Brittany O'Brien, Mark A Smith, Alan C Swann, Sanjay J Mathew, Nicholas Murphy, Marijn Lijffijt, Nithya Ramakrishnan, Bylinda Vo-Le, Brittany Vo-Le, Sidra Iqbal, Tabish Iqbal, Brittany O'Brien, Mark A Smith, Alan C Swann, Sanjay J Mathew

Abstract

Rapid antidepressant effects associated with ketamine have shifted the landscape for the development of therapeutics to treat major depressive disorder (MDD) from a monoaminergic to glutamatergic model. Treatment with ketamine, an N-methyl-D-aspartate (NMDA) receptor antagonist, may be effective, but has many non-glutamatergic targets, and clinical and logistical problems are potential challenges. These factors underscore the importance of manipulations of binding mechanics to produce antidepressant effects without concomitant clinical side effects. This will require identification of efficient biomarkers to monitor target engagement. The mismatch negativity (MMN) is a widely used electrophysiological signature linked to the activity of NMDA receptors (NMDAR) in humans and animals and validated in pre-clinical and clinical studies of ketamine. In this review, we explore the flexibility of the MMN and its capabilities for reliable use in drug development for NMDAR antagonists in MDD. We supplement this with findings from our own research with three distinct NMDAR antagonists. The research described illustrates that there are important distinctions between the mechanisms of NMDAR antagonism, which are further crystallized when considering the paradigm used to study the MMN. We conclude that the lack of standardized methodology currently prevents MMN from being ready for common use in drug discovery. This manuscript describes data collected from the following National Institutes of Health (NIH) and Veterans Affairs (VA) studies: AV-101, NCT03583554; lanicemine, NCT03166501; ketamine, NCT02556606.

Conflict of interest statement

VistaGen Therapeutics provided the AV-101 and placebo capsules and analyzed AV-101 metabolites (AV-101 study).

Biohaven Pharmaceuticals provided the investigational drug for the lanicemine study.

SJM has served as a consultant to Alkermes, Allergan, Axsome Therapeutics, Clexio Biosciences, Greenwich Biosciences, Intra-Cellular Therapies, Janssen, Neurocrine, Perception Neurosciences, Praxis Precision Medicines, and Sage Therapeutics. He has received research support from Biohaven Pharmaceuticals and VistaGen Therapeutics. ML has served as principal investigator for trials funded by NeuroRx and Vistagen Therapeutics and has received financial support from the MEDVAMC and the Department of Defense. MAS is an employee of VistaGen Therapeutics. The authors report no conflicts of interest.

Figures

Figure 1. Outline of the cortical response…
Figure 1. Outline of the cortical response to the generic mismatch negativity (MMN) paradigm. A) The schematic demonstrates the frequency and nature of an oddball stimulus over time. B) The solid black trace represents the grand average of the standard trials contrasted with the grand average of the deviant trials (dashed line) and the difference between them (deviant minus standard, solid red line). The MMN appears within the 150 to 220 ms window and reflects the extent of the deviation between the two conditions. C) Topographic response to each condition as recorded using a 64-channel EEG cap (10-20 montage).
Figure 2. Schematic depiction of an NMDA…
Figure 2. Schematic depiction of an NMDA receptor (NMDAR). Mechanisms of NMDAR antagonists can include blockade of subunits NR2B and NR1 (competitive antagonists), blockade of the glycine binding site (glycine antagonists), blockade of allosteric sites (noncompetitive antagonist), and blockade of the pore (uncompetitive channel blockers). The MMN appears to be affected by all types of NMDAR antagonists, indicating a generic role of NMDAR activation within its circuitry. Lanicemine and ketamine are channel blockers with different trapping block profiles. Ketamine exhibits the strongest and lanicemine the weakest trapping block. AV-101 (4-chlorokynurenine [4-Cl-KYN]) blocks NMDAR activity through competitive antagonism of the glycine-binding site.
Figure 3. Summary of the mismatch negativity…
Figure 3. Summary of the mismatch negativity (MMN) findings from the AV-101 (4-chlorokynurenine [4-Cl-KYN]) investigation. The MMN is visualized as a waveform corresponding to the difference between the standard and the deviant event-related potential (ERP) waveforms (red). The plots show data averaged across the measurement time points for the placebo group, low-dose group, and high-dose group (right). Black = standard ERP; blue = deviant ERP.
Figure 4. Summary of the mismatch negativity…
Figure 4. Summary of the mismatch negativity (MMN) findings from the lanicemine investigation. The MMN is visualized as a waveform corresponding to the difference between the standard and the deviant event-related potential (ERP) waveforms (red). The plots show data averaged across the measurement time points for the placebo group (left) and lanicemine group (right). Black = standard ERP; blue = deviant ERP.
Figure 5. Summary of the mismatch negativity…
Figure 5. Summary of the mismatch negativity (MMN) findings from the ketamine investigation. The MMN is visualized as a waveform corresponding to the difference between the standard and the deviant event-related potential (ERP) waveforms (red). The plots show data averaged across the measurement time points for the placebo group (left) and ketamine group (right). Black = standard ERP; blue = deviant ERP.

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