Evolutionary Insights into Hemispheric Switching from Bird Song:
I have always been intrigued by the possible role of interhemispheric switching in mating:- A spasm of Left hemisphere activation is seen in both mania and limerence (or acute erotic intoxication, the altered, transformative aspect of love made famous by the Bard and many others); fMRI studies show that the switch (VTA.ventral tegmental area) is strongly lateralised in limerence, switching sides when images of the love object are exchanged with those of less important people; courtship features strongly lateralised behaviour like poetry and song; etc.
These hints are a bit vague, but now Rod Suthers have provided a concrete example of the role of interhemispheric switching in the sexual behaviour of song birds.
Male canaries of some breeds use a “sexy” call to court females. This call is difficult to produce, as it varies at least three different measures:- band width, mean frequency and repetition rate of syllables. The Left hemisphere deals with low frequencies and the Right hemispheres deals with the high frequencies. The sexy call has a number of rapidly repeated low frequency syllables, produced by the Left, that are followed almost instantaneously by a high frequency note from the Right. Since the Left’s rapid series of notes is all generated by a single exhalation through the vocal tract on that side, that side is “out of breath” by the time of the following note generated by the other side. One can therefore see that a pretender that was trying to cheat the female by copying the sexy call, without the benefit of interhemispheric switching, is likely to be detected by a female who recognises the virtuosity that comes with switching. There are other examples in Suthers’ study, but the one I have chosen here makes it very clear that a timely production of a high note immediately after a rapid, breath-depleting succession of syllables would be impossible without the intervention of the other hemisphere.
I particularly like this example, because the implications of switching are usually most obvious for the human “switcher”, but here we see that the female canary must be aware of the some aspects of the switching process in another individual. I wonder if this is true for humans. Perhaps that feeling of being “in sync” with another has something to do with their having a similar switch rate so that switches (e.g. between send and receive) are more likely to be coordinated.
Zahavi was perhaps the first to clearly enunciate the principle of “truth in advertising” when it comes to the flashy signals used to attract mates. He argued that the peacock’s tail may be a truthful indicator of good genes, not so much because of its superficial gaudy features, but because it signifies a male capable of success despite that enormous handicap dragging behind. Not many females would be silly enough to choose a mate because they had hung a sign around their neck saying “I have good genes”, so convincing the female may require a demonstration that the male can overcome a handicap that is measurable by the female. In the present example, the female canary has the benefit of the virtuoso bilateral coordination made possible by the interhemispheric system to pick a male whose overall fitness may mirror that motor demonstration.
J Exp Biol. 2012 Sep 1;215(Pt 17):2950-9. doi: 10.1242/jeb.071944.
Detailed accounts of this work can be found in the following papers:-
switching mediates perceptual rivalry:
Steven M. Miller, Guang B. Liu, Trung
T. Ngo*, Greg Hooper, Stephan Riek, Richard G.
Carson, John D. Pettigrew Current Biology 10:383-392 2000 pdf
We have been lucky enough to have the article featured on the front cover. click here to see front cover.
2. Searching for the switch: Neural Bases
for Perceptual Rivalry Alternations.
John D. Pettigrew Brain and Mind:
A special issue on binocular rivalry (in press) click here to see
In this paper I outline my reasons for abandoning the idea that rivalry switches originate in visual cortex in favour of a more encompassing model of switching that involves the brainstem.
A midbrain neural basis for the perceptual oscillations of binocular rivalry is suggested on the basis of fMRI studies of rivalry and inferences from the properties of rivalry that cannot be explained from the known properties of primary visual cortical (V1) neurons. The rivalry switch is proposed to activate homologous areas of each cerebral hemisphere
alternately by means of a bistable oscillator circuit that straddles the midline of the ventral tegmentum. This bistable oscillator operates at the slow rate that is characteristic of perceptual rivalry alternations. Whilst aiming to divert the present preoccupation with cortical mechanisms for rivalry, the new proposal also integrates many cortical areas, in keeping with recent evidence that binocular rivalry involves widespread areas of the hemispheres. By linking rivalry to interhemispheric switching mechanisms in this way, the new proposal for the switch makes the surprising prediction that binocular rivalry will be subject to high level influences such as mood and motivation. These predictions are being fulilled, with rivalry playing an increasing role in the diagnosis and understanding of mood disorders and schizophrenia.
We show that two different hemispheric activating techniques produce changes in perceptual rivalry that are consistent with the hypothesis that the perceptual switches are mediated by attentional switches between the hemispheres. One method of unihemispheric stimulation is crude but long-lasting, an appropriate first experiment....caloric vestibular stimulation. Some subjects who received this treatment stopped switching between the two perceptual alternatives altogether!! The majority showed increases in the bias for one of the alternative perceptual states that were predictable if the two hemispheres were alternating percepts. The second method, transcranial magnetic stimulation, has great temporal precision and allowed us to probe precisely at the time of a perceptual switch. We found that we could disrupt perceptual rivalry in most subjects in a very specific way. ......only when the phase of the perceptual switch matched the hemisphere being stimulated. The phase specificity of the effect was a powerful control for other side effects of TMS, since the experimental disruption was seen only for one phase of the perceptual alternation.
This idea is not new. For example, ancient mystics were aware that their open nostril switched from side to side over hours as mood changed. Our new idea is to propose that binocular rivalry is a manifestation of interhemispheric switching.
Before our study there were a number that have cast increasing doubt over the popular notion that perceptual rivalry is mediated by the activity of neurons in primary visual cortex (V1). The reasons for eliminating V1 as the site of rivalry, and instead looking at higher levels, include the following:-
1. No evidence from monkey electrophysiology that V1 is the site; neurons with appropriate behavior are found in IT, not V1.
2. Monocular adaptation experiments fail to show teh effects predicted on rivalry if V1 is involved.
3. Eye swapping experiments: Rivalrous stimuli are exchanged rapidly between eyes with no effect on rivalry; V1 neurons are definitely affected
4. Synthesis (Diaz-Caneja, Kovacs): Rivalry shows reconstructive ability that has never been reported for V1:
5. Too slow (Sagar): The attentional spotlight in V1 is very fast (~30HZ), much faster that the changes in rivalry (~0.6-0.1Hz)
6. Henispheric activation/disruption: Experiments using caloric stimulation and TMS reported here.
7. PET/fMRI etc: None of these methods is yet fast enough to catch a switch; but the locus of activity is widespread and not specially V1.
8. Monocular rivalry and perceptual rivalry:
The new insights come from:-
Rama's studies of anosognosia show that the left hemisphere has a cognitive style that involves the denial of discrepancies that do not fit the overall plan "woven" by that hemisphere. The right hemisphere, in contrast, is looking for discrepancies while it monitors all inputs in a cognitive style that is reminiscent of a devil's advocate.
Each of these styles is valid (think of a mink pursuing prey visually while keeping a brief intermittent lookout for its own predators). The styles are fundamentally incompatible with the other if both are considered simultaneously. We have therefore proposed a switch between the two hemispheres, a bistable oscillator (see Figure) with the timing of the oscillator a sophisticated function of the many variables that have to be balanced (e.g. time of day, season, reproductive status, cognitive estimates of degree of security, etc.).
The hypothesis: A bistable neuronal oscillator in the brainstem switches "attentional mechanisms" between the hemispheres. The bistable oscillator involves paired neuronal structures with mutual inhibition between them, and depolarising cationic currents whose magnitude determines the rate of the switch.
In this fish, an interhemispheric switch is visible to the eye, without specialised equipment. The visual pathway is totally crossed. Saccades in one eye alternate with saccades in the other.
When two conflicting percepts are presented simultaneously, one to each eye, binocular rivalry ensues, with successive alternations of perception between the two possibilities. Binocular rivalry has traditionally been assumed to be mediated by reciprocal inhibition of neurones in separate monocular channels in primary visual cortex. Recent psychophysical and single-unit studies suggest however, that the site of rivalry is at much higher levels in the visual pathway, akin to attention. We use a Vision Works display and liquid crystal shutters to present horizontal moving stripes to the right eye while we simultaneously present vertical moving stripes to the left eye. The liquid crystal shutters allow the fields of view for each eye to be superimposed, with both horizontal and vertical targets occupying the same spatial location, so no special training in fixation is required. Subjects can accurately and successfully report rivalry within a few minutes of initial stimulus presentation.
Hemispheric Basis of Rivalry: Experiments we have carried out using unilateral caloric vestibular stimulation and transcranial magnetic stimulation during binocular rivalry suggest that the site of rivalry is at the level of the cerebral hemispheres themselves. We have therefore suggested that during binocular rivalry, each hemisphere adopts one of the rivalling stimuli and that competition for perceptual awareness occurs across rather than within the cerebral hemispheres.
a. Caloric Stimulation:(click here for details of protocol). Evidence for an interhemispheric switch in binocular rivalry comes from our experiments using unilateral cold caloric vestibular stimulation. PET and fMRI scanning have shown that caloric stimulation activates structures in the contralateral hemisphere that are implicated in attentional processing. In patients with right-hemisphere lesions causing left unilateral neglect and anosognosia (denial of illness), cold caloric stimulation of the left semicircular canals (activating the lesioned right hemisphere) can temporarily ameliorate visual and somatosensory neglect, and anosognosia. Since the caloric stimulation obviously has an effect on attentional processing in the clinical contexts of neglect and denial, and since imaging studies confirm the unilateral activation pattern induced by this technique, it can be used to assess whether rivalry is mediated by interhemispheric switching. A hemisphere-stimulating technique like caloric stimulation would have no effect on rivalry characteristics if rivalry is a within-hemisphere competition phenomenon. If, however, rivalry occurs across the hemispheres, then caloric stimulation should alter rivalry characteristics. This is exactly what we have found. The ratio of time spent in one perceptual state versus the other (ratio of the time spent "in" each hemisphere) can be increased or decreased by stimulating the right or left ear
b. Trans-cranial Magnetic Stimulation: A brief intense electro-magnetic pulse can activate superficial brain structures when applied across the skull. The brevity and sharp spatial localisation of the stimulation produced makes this technique ideally suited to test our interhemispheric switching hypothesis during binocular rivalry. In pilot experiments we obtained striking confirmation of the hypothesis. Application of a TMS pulse to one hemisphere (temporo-parietal region) had a disruptive effect on rivalry which was phase-specific. For example, left hemisphere stimulation, applied just as the percept was switching from vertical to horizontal, caused a brief reversion to vertical. There was no effect of the same stimulation when the TMS pulse was timed to occur at the opposite switch. The phase-specificity was reversed when the opposite hemisphere was stimulated. In summary, the results conform to expectations that flow from our interhemispheric switching hypothesis.
Idealised TMS experiment: (For picture of set-up,
Subject signals which of the two rivalling percepts is being experienced (upper trace). TMS is applied to a coil positioned over the left temporo-parietal region at each of the two different phases of perceptual shift.
1. When the pulse is applied as the perception is shifting towards the percept represented in the left hemisphere, there is a disruption of the "new" perception and a shift back to the previous perception. The duration of this disruption varied with subject and with intensity of stimulation. Some subjects saw a brief flash of the recent stimulus, others switched completely back to the previous stimulus.
2. When TMS was apllied at the opposite phase (second TMS pulse in bottom trace) there was no effect on the rivalling stimuli.
It is difficult to account for this phase-specific effect unless the rivalling percepts are represented in opposite hemispheres. The brief disruption caused by TMS is consistent with other effects of TMS (such as the brief scotomata induced by TMS of V1), if one percept, but not the other, is represented in the hemishere that was stimulated.