“Up the airy mountain, down the rushy glen, we dare n’t go a-hunting for fear of little men.” 
—From “The Fairies” by William Allingham—also said to Charlie outside of Willy Wonka’s Chocolate Factory 

It is a shame that we are getting so lazy in the way that we hunt for research regarding the brain. If a piece of research were published more than 10 years ago, it is almost as if it didn’t happen, and forget about going to read a book. A quick Google search and off we go to our next great idea—but it didn’t used to be this way, and for good reason. Take the genitalia for example (consider all childish puns here forward to be “intended”).

This is a story about how we should carefully read the old literature to better understand how researchers thought about the brain, and perhaps how we might question our assumptions about the brain. We might understand how errors can arise in our own data, and how to correct them—we might even learn something surprising. We also might learn something about the role novel ideas and creative thinkers play in the advancement of science more generally.

For example, Wilder Penfield and Herbert Jasper did some truly amazing research regarding cortical localization of function in the early part of the last century. They used a technique called “awake craniotomy”—a seemingly horrifying technique (that I participate in!) involving waking patients from anesthesia while undergoing brain surgery to map out regions of the brain the patient appears to be using, while removing damaged tissue. Since the brain itself does not have pain receptors, you can place an electrode on the cortical surface to interrupt ongoing neuronal activity to determine what tissue is critical to behavior, such as moving a limb or speaking. 

Which gets us to the “homunculus” (Latin for “little man”) that “lives” in the human brain. The homunculus is a cartoon (below) that represents the amount of brain tissue that is devoted to sensory or motor functioning in the human brain. For example, larger lips and hands represent the significant tissue devoted to these “sensitive” appendages.

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Penfield and Jasper wrote a book in 1954 entitled Epilepsy and the Functional Anatomy of the Human Brain in which they describe surgeries performed on some 750 patients undergoing awake craniotomy. Both males and females were studied, although only about 10 percent were female. With respect to the genitals, Penfield and Jasper state (page 69), “The representation of genitalia is only sensory and not motor.” Second, and importantly, they state, “Its relationship to foot is not altogether clear,” although they place the genitalia next to the foot on the sensory map (see above). Well there’s the rub …

I harken back to a brilliant talk that I attended in graduate school by V.S. Ramachandran at the International Neuropsychological Society (I still have the cassette tape, for those of you who remember such archaic technology, that I bought because I was so taken by the scope of his brilliance). He talked about Indian art, about creativity, and about foot fetishes. That is just how brilliant Ramachandran was and is: you see, he hypothesized that the proximal location of the foot right next to the genitalia on the homunculus, combined with a little “miswiring,” could lead to confusion between the pleasure felt from sexual stimulation and that felt from, say, toe sucking (he likely did not use such low-brow terms). 

But why would the genitals be “tucked away,” if you will, at the end of the homunculus instead of represented in the proper place—and in the rather orderly progression of all the other physical features of the human body? To be more specific, why aren’t the genitals located between the stomach and upper thigh where they “should” be? It turns out there are conflicting findings about the location of the genitals even in the classic literature, with Pfeifer (1920) finding them in the “correct” location between leg and trunk, Foerster (1936) finding them on the mesial paracentral lobule (below the toes), and Penfield et al. ascribing them to regions below the toes (1950). Wandering uterus indeed.

Perhaps it comes down to sex. A powerhouse review (Di Noto et al., 2013) notes that Penfield and his colleagues ascribe their “female” localization of the genitals to regions beyond the toes to a single case, a woman identified as “E.C.” who experienced sensory seizures involving her left labium and left breast. According to Di Noto, she is the only female patient of 107 that reported genital sensation following stimulation of the cortex! Di Noto and her colleagues advocate the creation (and provide a first approximation) of a “hermunculus” (which maps the female body in the brain), given the dearth of knowledge of female anatomy provided from the Penfield studies. But surely it’s not all cocked up you say? We have modern neuroimaging to show the way, yes?

Indeed, there are two studies that have emerged recently that are most informative to the current discussion. The first is by Kell et al., (2005) who studied the brains of 8 male subjects during “rest” and during stimulation of the penis with an “ultrasensitive” toothbrush (Dr. Best Flex Sensitive for those of you looking for a new fetish). They found that stimulation activated regions overlapping that of the lower abdominal wall, right where the “penis” would be expected. This result was found in each and every subject; thus their adapted homunculus would look like this (penis in right place):

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A second paper by Michaels et al., (2009) studied the brains of 15 women during “electrical dorsal clitoral nerve stimulation” (not experienced as pleasurable). They found that stimulation resulted in activation (compared to rest) in S1 (the white circled areas below), also not extending into the mesial wall—again, where it “should” be. Neither of these studies supports Penfield and Jasper’s homunculus.

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OK, what about sexual stimulation? Of course, neuroscience pushes ever forward with studies designed to satisfy our desire to know. In a comprehensive meta-analysis of male sexual arousal (Poeppl et al., 2013), 20(!) studies could not really tell whether the somatosensory cortex was active at all, although many, many other regions of the brain were active. In women, positron emission tomography was used to study the brains of 12 subjects during rest, and during clitorally induced orgasm (Giorgiadis et al., 2006), also resulting in broad activation patterns, as well as discrete activation in the dorsal primary somatosensory cortex, between the belly and thigh (below).  

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 Neither of these studies supports the “received” homunculus, and now both studies of passive stimulation and active sexual arousal suggest cortical maps that conform to human body architecture.  

So, what does it all mean for 1) genitals, 2) the brain, 3) Penfield, and 4) Ramachandran? With respect to the genitals, they look to be where they are supposed to be in the brain, and the cartoon of the little man should likely be updated so that he is not tripping over his junk. Second, the brain appears to be organized in a somatotopical manner (that means it roughly maps to the body in terms of location and importance of function). Third, Penfield and Jasper (among others) were studying people with epilepsy, tumors, and any number of other brain disorders, and some miswiring might be garbling the data, along with the highly possible reticence on the part of either the good doctors or patients to map or report stimulation regarding the genitalia as compared to ANY other sensory or motor function. And finally, Ramachandran remains a genius. He was likely wrong on this front, but he has brilliantly demonstrated a key feature of highly creative individuals: they put out a lot of ideas. Not all of them are right, but some might lead to a “novel and useful” treatment for phantom limb or a theory of synesthesia (the latter of which is well supported by “miswiring” data). Keep it sexy, Dr. R. …

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Literature cited:

Penfield W. & Jasper H. (1954) Epilepsy and the Functional Anatomy of the Human Brain. Little, Brown and Company, Boston, MA.

Di Noto, P, Newman L, Wall S, & Einstein G (2013). The Hermunculus: What is known about the representation of the female body in the brain? Cerebral Cortex, 23: 1005-1013.

Kell CA, von Kriegstein K, Rosler A, Kleinschmidt A, & Laufs H (2005). The sensory cortical representation of the human penis: Revisiting somatotopy in the male homunculus. The Journal of Neuroscience, 25(25): 5984-5987. 

Michels L, Mehnert U, Boy S, Schurch B, & Kollias S. (2010). The somatosensory representation of the human clitoris: An fMRI study. NeuroImage, 49: 177-184.

Poeppl TB, Langguth B, Laird AR, & Eickhoff SB (2013). The functional neuroanatomy of male psychosexual and physiosexual arousal: A quantitative meta-analysis.

Georgiadis JR, Kortekaas R, Kuipers R, Nieuwenburg A, Pruim J, Reinders AATS, & Holstege G (2006). Regional cerebral blood flow changes associated with clitorally induced orgasm in healthy women. European Journal of Neuroscience, 24: 3305-3316.