The Neurocritic: It Seems Like I've Been Here Before

Help me, somebody help me
I wonder where I am

Everything's Gone Green
----New Order

Edward Wild begins his comprehensive review on déjà vu in neurology with a definition from the unorthodox¹ Dr. Vernon Neppe:

V M Neppe proposed a definition of déjà vu in 1983 as “any subjectively inappropriate impression of familiarity of a present experience with an undefined past”. The definition is precisely worded and provides useful insights into the phenomenon.
The word “any” is intended to convey aetiological neutrality, implying that the experience need not originate from any particular pathological entity, or indeed any cause at all.
The “subjectively inappropriate” nature of déjà vu is critical to its understanding, as it implies insight into the unusual nature of the experience. The subject simultaneously seems to recognise a situation, yet knows that recognition to be impossible. Taking this further, the definition implies (though does not state) that the subject will try to explain the sense of familiarity and struggle to pinpoint its source but, frustratingly, cannot do so.

The most commonly occurring instances of déjà vu in neurology are in people with temporal lobe epilepsy (Vignal et al., 2006). The famous neurologist John Hughlings-Jackson was the first to describe the "dreamy state" in 1888 (actual PDF!):

The variety of epilepsy alluded to is one in which (1) the so-called "intellectual aura" (I call it "dreamy state") is a striking symptom. This is a very elaborate or "voluminous" mental state. One kind of it is "Reminiscence"; a feeling many people have had when apparently in good health... Along with this voluminous mental state, there is frequently a "crude sensation" ("warning") of (a) smell or (b) taste; (or, when there is no taste, there may be movements, chewing, tasting, spitting, implying (?) an epileptic discharge beginning in some part of the gustatory centres), or (c), the "epigastric" or some other "systemic" sensation. ...the "dreamy state" sometimes occurs without any of the crude sensations mentioned...

Given the conflicting results of brain stimulation studies in epileptic patients (Mullan & Penfield, 1959;² Halgren et al., 1978; Gloor et al., 1982; Bancaud et al., 1994), there has been a debate over which structures are most critical for eliciting the "dreamy state", and whether the spread of electrical discharge to temporal neocortex is necessary. Vignal et al. (2006) conclude thusly:

In the dreamy state, the recalled memory can be recent or remote. The mechanism involved does not appear to be different for these two types, in that the discharge involves only the MTL structures [not temporal neocortex]. This permanent role for the hippocampus and amygdala tends to invalidate the model of memory consolidation proposed by Squire and Alvarez (1995)...
Déjà vécu and visual memories involving recent and remote memories can be explained by the role of the amygdala, the hippocampus and rhinal cortex, whether right or left-sided, in the mechanisms of episodic autobiographical memory. The connections between these structures organize the content and the elaboration of the dreamy state for both remote childhood and recent memories.

These authors also point out that there is a continuum between déjà vécu (the more encompassing term meaning having lived through something before) and visual memory, both of which can occur during spontaneous seizures.

An interesting case study of déjà vu in a patient without temporal lobe epilepsy was reported by Kovacs et al. (2009). The patient, a 22 year old woman, was undergoing deep brain stimulation (DBS) to treat dystonia, a painful movement disorder involving involuntary muscle contractions and contorted posture. Due to a perinatal injury, she developed hemidystonia in her right arm. A stimulating electrode was implanted in the left internal globus pallidus (GPi), one of the output nuclei of the basal ganglia. Numerous papers have demonstrated that DBS in the GPi is effective in relieving the symptoms of dystonia.

Fig. 1 (Kovacs et al., 2009). Localization of the stimulating electrode: (A) coronal MP-RAGE, (B) coronal FLAIR, (C) sagittal MP-RAGE. Visual inspection and application of the electronic version of the Schaltenbrand stereotactic atlas verified that the contact responsible for DV [déjà vu] was situated between the GPi and the underlying white matter. The electrode did not hit the mesial temporal structures.

When stimulation at the deepest contact was turned on, the patient reported déjà vu phenomena:

Preoperatively the patient had never experienced DV. Immediately after turning on the DV-inducing stimulation, she experienced an unusual and obscure feeling. In addition to discomfort and a slight disturbance, the subject had an intact sense of reality; she was able to observe what was going on around her and to maintain verbal and behavioral responsiveness. We defined this period as the standby state for DV (SSDV). The SSDV persisted until stimulation of contact 0 was turned off or the amplitude of stimulation was lowered below 2.7 V.
During SSDV, she experienced impulse DV episodes lasting 4–5 seconds. On these occasions she felt that the situation seemed familiar. No visual or auditory illusions or hallucinations accompanied the DV. In addition, the patient felt neither the ability to predict the future nor unreality about current circumstances.

A SPECT (single photon emission computed tomography) scan was performed during one of the DV stimulation sessions. Like its more expensive cousin PET (positron emission tomography), SPECT measures cerebral blood flow, albeit with lower spatial resolution than PET. Structures in the right medial temporal lobe (contralateral to the stimulating electrode) showed greater blood flow during DV (as did other regions):

Compared with the baseline, SPECT during DV revealed right-sided hyperperfusion of the hippocampus, parahippocampal gyrus, fusiform gyrus, cerebellum, and temporal superior pole, and left-sided hyperperfusion of the cerebellum, operculum, insula, lingual gyrus, precuneus, and middle temporal gyrus. Hypoperfusion appeared bilaterally in the precentral and postcentral gyri, as well as in the frontal (especially supplementary motor cortex) and parietal areas.

Since no other cases of déjà vu have been reported in patients undergoing similar DBS, Kovacs and colleagues speculated that atypical neuroanatomy might have contributed to the phenomenon in this individual. An MRI prior to surgery showed right hemisphere dominance for language. In addition, they speculated on a possible functional relationship between the hippocampus and the contralateral basal ganglia, based on studies in rats. But overall, the authors admit they can't explain the pathophysiology of this unique DBS-evoked déjà vu.

Footnote

¹ Unorthodox, to say the least. Check out "vortex pluralism" -- his bizarre hypothesis to solve the mind-body problem.

² For more on these classic stimulation studies, check out Wilder Penfield, Neural Cartographer.

References

Bancaud J, Brunet-Bourgin F, Chauvel P, Halgren E. (1994). Anatomical origin of déjà vu and vivid ‘memories’ in human temporal lobe epilepsy. Brain 117:71–90.

Gloor P, Olivier A, Quesney LF, Andermann F, Horowitz S. (1982). The role of the limbic system in experiential phenomena of temporal lobe epilepsy. Ann Neurol 12:129–44.

Halgren E, Walter RD, Cherlow DG, Crandall PH. (1978). Mental phenomena evoked by electrical stimulation of the human hippocampal formation and amygdala. Brain 101:83–117.

Hughlings-Jackson J. (1888). On a particular variety of epilepsy (“intellectual aura”), one case with symptoms of organic brain disease. Brain 11:179–207

KOVACS, N., AUER, T., BALAS, I., KARADI, K., ZAMBO, K., SCHWARCZ, A., KLIVENYI, P., JOKEIT, H., HORVATH, K., & NAGY, F. (2009). Neuroimaging and cognitive changes during déjà vu. Epilepsy & Behavior, 14 (1), 190-196. DOI: 10.1016/j.yebeh.2008.08.017

Mullan S, Penfield W. (1959). Illusions of comparative interpretation and emotion: production by epileptic discharge and by electrical stimulation in the temporal cortex. AMA Arch Neurol Psychiatry 81:269–84.

Neppe V. (1983). The psychology of déjà vu: have I been here before? Witwatersrand University Press, Johannesburg.

Squire LR, Alvarez P. (1995). Retrograde amnesia and memory consolidation: a neurobiological perspective. Curr Opin Neurobiol 5:169–77.

Vignal JP, Maillard L, McGonigal A, Chauvel P. (2006). The dreamy state: hallucinations of autobiographic memory evoked by temporal lobe stimulations and seizures. Brain 130:88-99.

Wild E. (2005). Déjà vu in neurology. J Neurol. 252:1-7.