I’m not crying; it’s just been raining on my face

Posted by Xi Jiang on September 15, 2016 in Behavioral Neuroscience, Emotions, Neuroscience | Leave a comment

Humans and turtles have many things in common: we both possess four limbs, two eyes, a shell around our most vulnerable secrets, and tears that are attractive to butterflies and bees [1,2]. Our salt-rich tears, it seems, are much more palatable (and nutritious) to insects than they are to ourselves.

Julia butterflies drinking turtle tears [a].

That is not to say we ourselves have little use for tears; quite the contrary: reptilian tears originate from salt glands and are crucial for homeostasis, i.e. salt-water balance [3], while mammalian tears fulfill crucial eye-protective functions [4]. Our tear glands secrete “basal tears” constantly, to cover the eye with a water-based lubricant containing, among other things, anti-bacterial enzymes [5]. We also produce “reflex tears”, a term denoting increased fluid production due to irritation of the eye by foreign objects, such as dust, needles, and onion vapour. These irritants trigger the ophthalmic nerve to stimulate our tear glands and the conjunctiva lining the inside of the eyelids, opening the floodgates in a sometimes futile (e.g. against the death curse of an onion) attempt to wash the irritants away [6].

But when we think of tears, we seldom think of such mundane yet indispensable features like irritant-removal. Because we humans are such special snowflakes in the animal kingdom, we can perform odd physiological feats that seemingly make little biological sense, such as following a paleo diet, playing football, and crying under the influence of strong emotion. Crying, or “emotional lacrimation” (“lacrima” being the Latin word for “tears”), can be described in an utterly boring fashion as “a complex secretomotor phenomenon characterized by the shedding of tears from the lacrimal apparatus, without any irritation of the ocular structures” [7]. What this technical definition does not tell us, however, is how exactly crying happens beyond the mechanical level. The observation that humans seem uniquely “gifted” with the ability to cry [8] also begs explanation. We can often easily point to the external and immediate cause of our tears: a movie about a loyal dog ends with both the dog and the master dead, a person who is supposed be “the one” turns out to be “the other”, the Grand Canyon is so very big it literally brought water to the eyes, etc.. But what is the point of over-lubricating our eyes when we are sympathetic, heartbroken, or awestruck?

Left: Movie poster for “Hachiko Monogatari” (“Hachiko’s Story”), 1987. Text: “Hachi kept waiting/For the return of dear Master” [b]. Right: the historical Hachiko, whom the movie was based on [c].

Barring the Internet hypothesis that a highly trained team of covert operatives are dispatched across the globe to cut onions strategically, how would we explain the phenomenon of crying? While even infants are capable of crying, often to the detriment of their future loved ones, their crying is most likely an innate and reflexive behavior meant for signaling the parents, and may be evolutionarily conserved among mammalian species [9]. This is quite different from the emotional lacrimation seen in adults, who are capable of crying over a much wider emotional spectrum for sometimes obscure reasons. To investigate the physiological roots of “post-baby crying”, then, one would need to focus on the emotional aspect, whereby neuroscience gives us a few obscure, but discernible, hints.

One straightforward, if overly reductive, idea is that we simply “supercharge” our baby-crying prowess as we grow up. That is to say, adult-crying may serve the same purposes as baby-crying: a social signal of need/distress—a primordial “Help Me” [10]. For both parents and non-parents, fMRI studies showed that human infant faces and cries preferentially activated certain cerebral structures compared to animal images and infant cries played backwards. Those structures include amygdala and anterior insula, both important structures for assigning emotional context to experience [11]. The same brain regions are also more active when adult humans listened to adult crying and, interestingly, adult laughter, than when listening to played-backward crying/laughter cues [12].

While provocative, there are at least two significant difficulties with the “Help Me” theory: first, as mentioned before, emotional crying in adults does not appear in our close evolutionary cousins, such as other existent primates [8]. Second, just because similar brain regions are involved in processing infant and adult crying, it does not follow that they would have the same behavioral influence, or even involve the same brain regions elsewhere at earlier/later stages of information processing. In fact, compared to adult poker faces (“non-emotive” in Academese), infant poker faces elicit much greater responses in the anterior insula of human parents and the additional involvement of the supplementary motor area [13], a brain region recently reported to be crucial in rapid differentiation between infant and adult vocalization [14]. In short, our brains’ reactions to infant versus adult crying have some similarities, but are not nearly similar enough to be considered the same. In addition, we are still left with the puzzling observation that “tears of joy” are, as they say, a thing. Why would an important social cue denote two extremely different emotions, only one of which would signal the need for assistance?

To be honest, like many other questions posited on this blog, we do not currently know enough to solve the “paradoxical tears” puzzle, either in an evolutionary or in a physiological sense. However, there does exist a new theory that shows a promising angle of attack. The lacrimal gland, our tear factory, is primarily connected to the lacrimal nucleus, which belongs to a group of neurons in the brain stem responsible for producing a variety of face fluids, such as saliva, mucus, and of course, tears. The lacrimal nucleus is in contact with a wide range of cerebral areas, among which is the hypothalamus [15], the key region for the aforementioned new theory.

Top: Cartoon of cerebrum showing the locations of hypothalamus and of pontine tegmentum, where the lacrimal nucleus resides [d]. Bottom Left: Partial sketch of nerves involved in human lacrimation. Blue arrows indicate direction of information flow [e]. Bottom Right: Sketch of the lacrimal gland (the globular structure to the northwest) in relation to the eye and tear ducts [f].

The hypothalamus is responsible for producing and distributing chemical signals (i.e. neurotransmitters and neurohormones) that lead to physiological effects of emotions, such as having one’s heart racing while in fear of a clown’s visage. Among the many hypothalamic signals is acetylcholine, which gets released in large amounts upon us experiencing extreme emotions, regardless of valence (Academese for “the goodness/badness of a thing”) [16,17]. The salty droplets on the corners of our eyes at weddings and reunions, therefore, might simply be an evolutionary accident: our lacrimal gland just happens to be sensitive to acetylcholine signaling [18], perhaps to a degree greater than in the average monkey.

Be it physiological accident or functional social cue, our emotional tears do have importance that transcends biology and makes the biological question interesting in the first place. With any luck, we should all have people who would one day cry for us, and not necessarily because we would no longer be around. It seems fundamentally human to have something, or someone, important enough to deserve our tears, and getting to know what makes us human—well, that just seems like the most human thing to do.

References:

[1] Hogue CL (1993). Latin American Insects and Entomology. University of California Press. pp. 457–. ISBN 978-0-520-07849-9.

[2] Bänziger H et al. (2009). Bees (Hymenoptera: Apidae) that drink human tears. Journal of the Kansas Entomological Society 82(2):135-150.

[3] Hildebrandt J (2001). Coping with excess salt: adaptive functions of external osmoregulatory organs in vertebrates. Zoology 104:209–220.

[4] Walcott B (1998). The lacrimal gland and its veil of tears

[5] Farandos NM et al. (2014). Contact lens sensors in ocular diagnostics. Advanced Healthcare Materials 4(6):792-810.

[6] Pan Z et al. (2012). Transient Receptor Potential (TRP) channels in the eye. Ch.3 in Advances in Opthalamology. INTECH. ISBN 978-953-51-0248.

[7] Patel V (1993). Crying behavior and psychiatric disorder in adults: a review. Compr Psychiatry. 34 (3):206–11.

[8] O’Bleness M et al. (2012). Evolution of genetic and genomic features unique to the human lineage. Nature Reviews Genetics. 13:853-866.

[9] Lingle S and Riede T (2014). Deer mothers are sensitive to infant distress vocalizations of diverse mammalian species. The American Naturalist. 184(4):510-522.

[10] Piallini G et al. (2015). Parental brain: cerebral areas activated by infant cries and faces. A comparison between different populations of parents and not. Frontiers in Psychology. 6:1625.

[11] Phan KL et al. (2002). Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI. NeuroImage. 16(2):331-348.

[12] Sander K and Scheich H (2005). Left auditory cortex and amygdala, but right insula dominance for human laughing and crying. Journal of Cognitive Neuroscience. 17(10):1519-1531.

[13] Caria A et al. (2012). Species-specific response to human infant faces in the premotor cortex. NeuroImage. 60(2):884-893.

[14] Young K et al. (2016). Evidence for a caregiving instinct: rapid differentiation of infant from adult vocalizations using magnetoencephalography.

[15] Van der Wert F et al. (1996). Innervation of the lacrimal gland in the cynomolgous monkey: a retrograde tracing study. Journal of Anatomy. 188:591-601.

[16] Jiang L et al. (2016). Cholinergic signaling controls conditioned fear behaviors and enhances plasticity of cortical-amygdala circuits. 90(5):1057-1070.

[17] Picciotto M et al. (2015). Mood and anxiety regulation by nicotinic acetylcholine receptors: A potential pathway to modulate aggression and related behavioral states. Neuropharmacology. 96:235-243.

[18] Mitchelson F (2012). Muscarinic receptor agonists and antagonists: effects on ocular function. Handbook of Experimental Pharmacology. 208:263-298.

 

Image sources:

[a]: By amalavida.tv, CC BY-SA 2.0, https://commons.wikimedia.org/w/index.php?curid=34852753

[b]: https://upload.wikimedia.org/wikipedia/en/4/42/Hachik%C3%B4_monogatari.jpg

[c]: https://upload.wikimedia.org/wikipedia/commons/6/6b/Hachiko.JPG

[d]: Blausen.com staff. “Blausen gallery 2014”. Wikiversity Journal of Medicine. DOI:10.15347/wjm/2014.010. https://commons.wikimedia.org/wiki/File:Blausen_0536_HypothalamusLocation.png

[e]: Plate 788, Gray’s Anatomy. https://commons.wikimedia.org/wiki/File:Gray788.png

[f]: Plate 896, Gray’s Anatomy. https://commons.wikimedia.org/wiki/File:Gray896.png

Featured image: https://pixabay.com/en/eye-tear-cry-sadness-pain-emotion-609987/