The old Jewish Cemetery; Venice, 1790. 

Goethe loosens the earth from the skull, and holds it up to the sun. 

Turning the fractured bone back and forth, he gasps.  A series of marks appear inside the cavity, reminding him of the vertebrae.  He has looked at this pattern many times, but without seeing what lights up before him today. 

Here is the shadow of a blueprint; the ‘primal repeating units’ of animal bodies, from which their many variations form. 

Puzzled, Götze watches his master’s eyes shine with delight. 

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Watch this baby babbling; her limbs move, often in time with her sounds.  the coupling of gestures and vocal calls are widespread amongst social vertebrates.  And the story began with fish.

The rhythm of our breath keeps us alive.  Conscious muscle movements are made through spinal nerve reflexes, but like our heart beats, the repeating sequences of muscle actions which fill and empty our lungs are outside our conscious awareness.

The movements behind repetitive activities like breathing are driven by rhythmic nerve impulses from ‘neural oscillators’.  These pattern-generating circuits, located in the central nervous system, are known as ‘Central Pattern Generators’.

To breathe, to speak and to swallow we use the same internal tube; that is our throat (the pharynx).  These activities are necessarily exclusive; consider what happens when a crumb ‘goes down the wrong way’.  Speech therefore needs to be coordinated with our breathing.

We make vocal sounds by passing air through the larynx as we breathe out, at the same time as vibrating our vocal folds (vocal cords).  These actions involve coordinating a sequence of repetitive movements inside the throat with the repeating muscle actions that drive our breath.

Communicating with sound evolved long before animals emerged from the sea onto land and began to breathe air.  Many fish use pectoral fin movements as communication gestures; some also generate sounds by fin waving.

In species of vocal fish, the calls are coordinated with these pectoral fin signals.  Significantly, the muscles operating these social communication cues are controlled using the same neural oscillator ‘module’.

‘Central Pattern Generators’ are neural oscillators that generate a rhythmic output, used to control repeating muscle movements.  These ‘neural metronomes’ were first discovered in insects, and produce their steady pulse without any sensory stimulus.  In contrast, our other nerves operate on a ‘stimulus-response’ basis.

 

Central Pattern Generators reveal what can be called our ‘deep homology’.  First discovered in insects, all vertebrates, including ourselves, have these ancient neural circuits.  They links vocal calls with gestures, and coordinate our ‘fins’ with our speech.

How do Central Pattern Generators work? 

We consciously control our limbs through spinal nerve reflex arcs.  In contrast, rhythmic movements controlling oscillating cycles are driven by Central Pattern Generators (CPGs).  These autonomous modules in the central nervous system produce a rhythmic output (like a neural ‘black box’).  CPG modules are comprised of a dense interconnected local network of neurons; a neural ‘node’.

These nodes are organised into three levels, each with a different function, and in each case, the parts of the circuit ‘higher’ in this organisation regulate the outputs of those below.

In the developing embryo there are functional units, ‘segments’ which give rise to our vertebrae and their associated nerves and muscles.  The nerves from each of these ‘segments’ form our local sensory spinal reflexes and also the CPG modules.  As needed, higher brain centres trigger these ‘neural motors’ to produce their rhythmical nerve impulses and drive all of our rhythmical movements from walking to chewing.

CPGs controlling rhythmic movements of the tongue, throat and breathing (including the vocal neural oscillator module) are in the lower brainstem and neck.  The CPGs that drive the rhythm of our walking are low down in the spinal cord, in the thoracic and lumbar regions.

Why don’t we sound like fish? 

Toadfish vocalise with either a sequence of repetitive grunts during aggressive encounters or the prolonged drone of their mating call.  In both cases, each nerve impulse from the vocal pattern generator produces a single synchronised contraction in their sonic muscles; this muscle pair flexes the rigid walls of the swimbladder, producing a ‘grunt’.  This sound receives no further processing.  As a result, its tone is rather mechanical.

Our voice, like that of frogs, birds and mammals, also begins with this simple rhythmic sound pulse.  This initial sound is then processed into croaks, calls songs and speech.  Our neck  allows us to create resonant areas in the throat which amplify certain frequencies.  Pitch is affected by vocal fold (vocal cord) tension, and manipulation of our tongue and lips produces precisely articulated words.

Why is ‘talking with our hands’ still a part of our language?

Many vocal fish make synchronised gestures with their front (pectoral) fins during mating calls.  These motor nerve connections from our ancient common ancestor are retained in other vertebrates.

People blind from birth move their hands when they talk.  Our vocal Pattern Generator circuits connects with both our larynx and pectoral muscles, coordinating our speech with our ‘body language’.  We subconsciously move our hands as we communicate thanks to these rhythmic central circuits.  As in all other vertebrates, we have inherited these from (as Palaeontologist Neil Shubin puts it) our ancestral ‘inner fish’.

Text copyright © 2015 Mags Leighton. All rights reserved.

References

Aboitiz, F. (2012)  Gestures, vocalizations, and memory in language origins.  Frontiers in Evolutionary Neuroscience 4, e2.

Bass, A.H. and Chagnaud, B.P. (2012)  Shared developmental and evolutionary origins for neural basis of vocal-acoustic and pectoral-gestural signalling.  Proceedings of the National Academy of Sciences, USA 109 (Suppl.1), 10677-10684.

Bass, A.H. et al. (2008)  Evolutionary origins for social vocalization in a vertebrate hindbrain-spinal compartment.  Science 321, 417-421.

Bostwick, K.S. (2000) Display behaviors, mechanical sounds, and evolutionary relationships of the Club-winged Manakin (Machaeropterus deliciosus). Auk 117, 465-478.

Bostwick, K.S. et al. (2010)  Resonating feathers produce courtship song. Proceedings of the Royal Society, B 277, 835-841.

Chagnaud, B.P. et al. (2012)  Innovations in motoneuron synchrony drive rapid temporal modulations in vertebrate acoustic signalling.   Journal of Neurophysiology 107, 3528-3542.

Dick, A.S. et al. (2012)  Gesture in the developing brain.  Developmental Science 15, 165–180.

Ghazanfar, A.A. (2013) Multisensory vocal communication in primates and the evolution of rhythmic speech. Behavioral Ecology and Sociobiology 67, 1441-1448.

Goethe, J.W. (1820).  Zur Naturwissenschaften überhaupt, besonders zur Morphologie; cited (p. 7) in G.R. de Beer The Development of the Vertebrate Skull.  Clarendon (1937).

Guthrie, S. (1996)  Patterning the hindbrain.  Current Opinion in Neurobiology 6,41-48.

Hanneman, E. et al. (1988) Segmental pattern of development of the hindbrain and spinal cord of the zebrafish embryo. Development 103, 49-58.

Iverson, J.M. and Thelen, E. (1999)  Hand, mouth and brain: The dynamic emergence of speech and gesture.  Journal of Consciousness Studies 6, 19-40.

Kelley, D.B. and Bass, A.H. (2010)  Neurobiology of vocal communication: mechanisms for sensorimotor integration and vocal patterning. Current Opinion in Neurobiology 20,748-53.

Marder, E. and Bucher, D. (2001)  Central pattern generators and the control of rhythmic movements.  Current Biology 11, R986-R996.

Shubin, N (2008)  Your inner fish; a journey into the 3.5 Billion year history of the human body.  Penguin Books Ltd.

Shubin, N. et al. (2009)  Deep homology and the origins of evolutionary novelty.  Nature 457, 818-823.

Upon leaving the island, Odysseus is warned that storms lie ahead. His route home to Ithaca passes the sirens; monsters whose beautiful, haunting voices lure sailors to their deaths.  

He sets a course and explains his intention to the crew. At his command they fasten him to the mast, seal their ears with wax, and prepare for their encounter.

They reach treacherous waters. The siren song reaches into Odysseus’ mind, resonating with his deepest longings. The storm rages within. He struggles, but his bindings, the result of his clear intention, secure him tightly to the mast.

Forced to stand still and listen, he finds that he starts to hear the voices for what they really are; the empty fears of his own soul. He relinquishes his fight and hears the voice at his own still centre. The storm calms.

The crew notice that he has returned to his senses. They cut him loose.

He is indeed a wise and worthy captain.

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Speaking involves transmitting and interpreting intentional signs, some of which are also used in the instinctual communications of animals. These signals are of three kinds: 1. An index physically shows the presence of something, e.g. wolves tracking their prey by scent.

2. An ‘icon’ resembles the thing it stands for, like a photograph or a painting. Dolphins, apes and elephants recognise their own reflection; we assume that they interpret this two-dimensional image as representing their three-dimensional physical selves.

3. A symbol associates an unrelated form with a meaning. Our words are symbols, linking an idea with unique sound-and-movement sequences. They do not resemble the things they represent.

Symbolism is almost unknown amongst animals, with a few rare exceptions. A stereotypical form of symbol is the ‘waggle dance’ of honeybees.

Although chimpanzees can be taught to use some sign gestures, they do not naturally communicate using symbols. In contrast, we use our symbolic language intentionally.

Our uses of speech are unique. We revisit our memories, order our thoughts and make future plans. With a destination in mind, we can listen for our ‘inner voice’, map out our route, take a stand against the storm of inner and outer distractions, and find our way home.

How is our speech unique?

Aspects of our language ability are found in other animals, but the way we have combined and developed these traits is uniquely human.

1.  We use any available channel.

Most human languages use vocal speech. Under circumstances where speaking is not possible, we find other ways, e.g. sign languages and Morse code.

2.  We build our words from parts that gain meaning as they are combined

Most of the syllables we use to build words lack meaning on their own. Combining them together (as in English) or adding tonal shifts (as in Chinese) creates words.

3.  We code our words with meanings, making them into symbols

Symbols are ‘displaced’, i.e. they do not need to resemble the thing they represent. Our words symbolise ideas, experiences and things.

4.  We combine these symbols to make new meanings.

We build words into phrases and stories, use these to revisit and share our memories, combine them into new forms, and communicate this information to others in various ways. Combining different symbols brings us a new understanding, which changes how we respond.

Look at this painting. As you do, consider what feelings it provokes.

It is, of course, by Vincent Van Gogh. As you may know, his choices of colour and subject material were a personal symbolic code. He often used vibrant yellows, considering this colour to represent happiness.

His doctor noted that during his many attacks of epilepsy, anxiety and depression, Van Gogh tried to poison himself by swallowing paint and other substances.

As a consequence, he may have ingested significant amounts of toxic ‘chrome yellow’, which contains lead(II) chromate (PbCrO₄).

Now consider this statement.

“This is the last picture that Van Gogh painted before he killed himself” (John Berger 1972, p28)

Look again at the picture.

What do you feel this time?

Certainly our response has changed, though it is difficult to articulate precisely what is different. The image now seems to illustrate this sentence. Its symbolic content has altered for us. This example shows how combining two types of information –an image and text- can change the meaning it symbolises.

Some animals can be trained to recognise simple symbols. The psychologist Irene Pepperberg taught her African Grey parrot ‘Alex’ to count; he learned to use numbers as symbols, and could identify quantities of up to 6 items.

5.  The order in which we combine symbols defines their meaning

We put word symbols together into phrases, sentences, descriptions, sayings, stories, poems, documents, manuals, plays, oaths, promises, parodies, plays, pantomimes….

The ordering of words follow rules (grammar and syntax). Animals such as dogs and dolphins show some form of syntactical ability, but there is no evidence that they are on the verge of using what we understand as language. The order of words shows us their relationship, allowing us to understand how they are interacting. We change the order of our words and phrases to change the meaning we wish to communicate.

For instance; this makes sense.

‘Jane asked Simon to give these flowers to you.’

This doesn’t quite fit our normal understanding of reality…

‘These flowers asked Simon to give Jane to you.’

This works, but the meaning has changed.

‘Simon asked you to give these flowers to Jane’

However grammar is not enough . The words in combination need to ‘make sense’ for us to understand the meaning the speaker wishes to communicate.

What does this enable us to say?

When we make new combinations of words, or add words to a visual signal such as a gesture, we create a new meaning.

We can add adjectives to a description, add qualifiers, combine phrases into a sentence, and make statements one after the other so that our listener associates these ideas. This process is known as ‘recursion’, a linguistic term borrowed from mathematics.

Our ideas about time vary between cultures, but we all mentally ‘time travel’ by revisiting our memories. For instance, the scent of something can evoke a memory that transports us back into an earlier event; suddenly we experience again the emotions and sensations we felt at that time. Putting our current selves into the past memory, or imagining a future scenario and inserting ourselves into that story, is a form of recursion.

Memory allows us to link speaking and listening with the meanings of our words. Our language is well structured to easily express recursive ideas. This shows us that our thinking uses recursion.

Why are we able to do this?

Our thinking capacity, through which we learn and remember, means that we can copy and learn to use language. Although some brain regions appear specialised for roles in memory and language, our ‘language function’ uses our entire brain, and cannot be dissociated from our minds.

Our ‘language brain’ includes the ‘basal ganglia’; these are neurons which connect the outer cortex and thalamus with lower brain regions.

We need this connectedness to coordinate movements in our fingers, to understand the relationships between words that are inferred by their order in our phrases, and to solve abstracted (theoretical) problems. This network interacts with ‘mirror neurons’ which allow us to relate to and decode the posture, speech and emotional cues of others.

The  basal ganglia that influence our speech also regulate the muscles controlling our posture. Standing is therefore more than just balancing on two legs; it is a whole body activity and requires much finer muscle control than walking on all fours. It also frees the hands, which allows us to manipulate tools. Lieberman suggests that it is the fine motor control required to maintain our upright posture which pre-adapted our ancestors for manipulating hand tools as well as the tongue, lips and other structures that make speech possible.  This upright posture is linked with a remodelling of our breathing apparatus, giving us more control over our larynx.

Philip Lieberman’s work with people suffering from Parkinson’s’ disease suggests that it is the ability to remember that makes speaking possible. Parkinson’s patients have degraded nerve circuits in their basal ganglia, so these patients have short term memory problems and difficulties with balancing and making precise finger movements. They also struggle with understanding and using metaphors and longer word sequences. This suggests that when we speak we are using the circuitry for sorting and remembering movement sequences, irrespective of whether these are producing words or actions.

 

The basal ganglia that influence our speech also regulate the muscles controlling our posture. Standing is therefore more than just balancing on two legs; it is a whole body activity and requires finer muscle control that walking on all fours.  It also frees the hands, which allows us to manipulate tools.

Lieberman suggests that it is the fine motor control required to maintain our upright posture which pre-adapted our ancestors for manipulating hand tools as well as the tongue, lips and other structures that make speech possible.  This upright posture is linked with a remodelling of our breathing apparatus, giving us more control over our larynx.

The nerve networks that control our limbs and voices are linked across all vertebrates. Our basic ‘walking instinct’ initially activates Central Pattern Generator circuits driving movement in all four limbs. These are the same neural outputs that control our lips, tongue and throat.

Conclusions: What does this say about our language?

• Our hominin ancestors evolved to use symbolic words and stories as a code to store and share memories, develop new skills and ideas, and coordinate their intentions and actions with their tribe.
• When we revisit our memories or ‘reword’ our experiences into new sequences, we remodel the past, and project our thoughts into the future.
• The control we have over our vocal sounds is linked with our neural circuits for movement. The ability to balance ideas and manipulate our tongues is linked to our ability to stand upright, balance on two feet and manipulate tools with our hands.
• Language, then, is a cultural tool that allows us to order our thoughts, go beyond our instincts, share our intentions, and choose our own story.

Text copyright © 2015 Mags Leighton. All rights reserved.

References

Berger J (1972) ‘Ways of Seeing’ Penguin books Ltd, London, UK

BickertonD and Szathmáry E (2011) ‘Confrontational scavenging as a possible source for language and cooperation’ BMC Evolutionary Biology 11:261  doi:10.1186/1471-2148-11-261

Corballis MC (2007) ‘The uniqueness of human recursive thinking’ American Scientist Volume 95 (3), May 2007, Pages 240-248

Corballis, M.C.(2007) ‘Recursion, language, and starlings’ Cognitive Science 31(4) 697-704

Everett D (2008) ‘Don’t sleep, there are snakes: Life and language in the Amazonian jungle’ Pantheon Books, New York, NY (2008)

Everett, D (2012) ‘Language: the cultural tool’ Profile Books Ltd, London, UK

Gentner TQ et al (2006) ‘Recursive syntactic pattern learning by song birds’ Nature, 440;1204–1207

A lone singer waits for darkness. 

Dusk falls.  As the waves push and pull at the sand with a steady rhythm, he revs up his vocal muscles for this, his love song. 

He begins to hum.  His baritone burr becomes louder and louder, booming across the bay.  After a few minutes, another voice joins in, slightly off pitch. 

They sing for over an hour.  Local residents head indoors, slamming windows to block out the noise.

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The male plainfin midshipman fish has evolved to sing; not for ‘fun’ but to attract females to lay their eggs in his rocky burrow.  The call advertises his suitability to safeguard first the eggs and later the juvenile fry.  We usually associate parental care with mammals and birds.  For these territorial nesting fish, protection improves the survival of young at their most vulnerable life stage, which confers a considerable selectable advantage.

However these male fish come in two forms.  These other males are smaller, look like females, and like females they don’t sing.  When a real female is present they enter the nest and release sperm in the hope of fertilising some of the eggs.  Extreme competition for nest sites and breeding partners is thought to have selected for the evolution of these ‘sneaker’ males.  Male ‘cross-dressing’ cuckolds have been found in other animal species with extreme between-male competition for mates, some cuttlefish, lizards and dung beetles.

Singing male midshipman fish develop larger and more complex networks of vocal neurons in the brain than non-singers.  These networks, together with others that control the sense of hearing,  become more sensitive when the levels of sex hormones rise in the fish’ body.  These chemicals peak during the spawning season, prompting the males to sing and making the females more responsive.

In some ways the fish brain is a simpler version of our own, and other tetrapods.  Studying differences between the brains of these singing and non-singing male fish shows us how mate selection may have first prompted our ancestors to evolve a voice.

How does the male midshipman fish make his song?

The plainfin midshipman is one of several species of vocal fish that nest in the intertidal zone, creating a linear ‘lek’ along the coast.  Singing males hum by contracting a pair of sonic muscles attached to the swim bladder.  This pressurised air sac, used for buoyancy, shares developmental origins with our lungs  and helps the fish amplify his own voice.  Fast, synchronised contractions of the sonic muscles vibrate this ‘stiff-walled balloon’, generating sounds.

All midshipman fish have sonic muscles.  In singing males these muscles are six times larger than in females and ‘sneaker’ males.  The singer’s muscle fibres are larger, four times as numerous, and surrounded by numerous mitochondria; the cell’s ‘power generators’.  Only these powerful muscles and a steady energy supply can sustain their hour-long mating call.

What inspires him to sing?

Singing males call only during the spawning season, and only at night.  The hormone melatonin, produced by the pineal gland, regulates this and other daily (circadian) and seasonal rhythms in the physiology and behaviour of vertebrates.  Longer hours of daylight in the spring lowers melatonin production, allowing the higher brain centres to release neurotransmitters.  These small protein signals trigger the production of sex hormones, which initiate nest building and singing behaviour in midshipman parental males.

Both singing and ‘sneaker’ males produce the male hormone testosterone.  However singers also produce a related chemical, 11-ketotestosterone, which enhances the performance of the vocal brain’s neural networks, and increases the growth of their sonic muscles.

The larger bodies of these singing males means they take longer to reach reproductive size, but potentially can mate with more females.  Sneaker males have the advantage of maturing quickly but the trade-off is that their reproductive success is uncertain.

How is the fish’s brain seasonally rewired for sound?

In singing males, seasonally high levels of 11-ketotestosterone make the vocal parts of the brain more responsive, prompting them to initiate their humming calls.  These brain regions contain ‘receptors’; that is protein ‘signal receivers’ that recognise the hormonal messages.  As the hormone binds, the receptor  changes shape into an active form and in turn modifies the genes which are employed by the vocal neurons to change their function.

In the part of the female fish’ ear that is the functional equivalent of our cochlea (the human hearing organ), oestrogen hormones are ‘seen’ by receptor proteins in a similar way. This renders her hearing more sensitive within the specific vocal range of the male’s droning call, enabling her to pick up its subtle nuances and high harmonics.

High oestrogen levels are also linked to better hearing in frogs and humans.

Text copyright © 2015 Mags Leighton. All rights reserved.

References

Arch, V.S. and Narins, P.M. (2009)  Sexual hearing: the influence of sex hormones on acoustic communication in frogs.  Hearing Research 252, 15-20.

Bass, A.H. (1990)  Sounds from the intertidal zone: vocalizing fish.  Bioscience 40, 249-258.

Bass, A.H. (2008)  Steroid dependent plasticity of vocal motor systems: novel insights from a teleost fish.  Brain Research Reviews 57, 299-308.

Bass, A.H. et al. (2008)  Evolutionary origins for social vocalisation in a vertebrate hindbrain-spinal compartment.  Science 321, 417-721.

Bass, A. H. (1996)  Shaping brain sexuality.  American Scientist 84, 352-363.

Fergus, D.J. and Bass, A.H. (2013)  Localization and divergent profiles of estrogen receptors and aromatase in the vocal and auditory networks of a fish with alternative mating tactics.  Journal of Comparative Neurology 521, 2850-2869.

Foran, C.M. and Bass, A.H. (1999)  Preoptic GnRH and AVT: axes for sexual plasticity in teleost fish.  General and Comparative Endocrinology 116, 141-152.

Knapp, R. et al. (1999)  Steroid hormones and paternal care in the Plainfin Midshipman fish (Porichthys notatus).  Hormones and Behavior 35, 81–89.

Moller, A.P. and  Briskie, J.V. (1995)  Extra-pair paternity, sperm competition and the evolution of testis size in birds.  Behavioral Ecology and Sociobiology36, 357-365.

Rubow, T.K. and Bass, A.H. (2009)  Reproductive and diurnal rhythms regulate vocal motor plasticity in a teleost fish.  Journal of Experimental Biology 212, 3252-3262.

Sloglund, C.R. (1961)  Functional analysis of swimbladder muscles engaged in sound production of the toadfish.  The Journal of Biophysical and Biochemical Cytology 10, 187-200.

Wilczynski, W. and Ryan, M.J. (2010)  The behavioural neuroscience of anuran social signal processing.  Current Opinion in Neurobiology 20, 754-763.