It has been clear for decades that aphasia never occurs without subcortical damage, and can occur absent insult to the cortex (Naeser et al. Reference Naeser, Alexander, Helm-Estabrooks, Levine, Laughlin and Geschwind1982; Stuss & Benson Reference Stuss and Benson1986). The speech production deficits of Parkinson disease and focal lesions to the basal ganglia are qualitatively similar to ones occurring in aphasia (Blumstein Reference Blumstein, Miller and Eimas1995; Blumstein et al. Reference Blumstein, Cooper, Goodglass, Statlender and Gottlieb1980; Lieberman et al. Reference Lieberman, Friedman and Feldman1990; Reference Lieberman, Kako, Friedman, Tajchman, Feldman and Jiminez1992; Pickett et al. Reference Pickett, Kuniholm, Protopapas, Friedman and Lieberman1998; Usui et al. Reference Usui, Inoue, Kimura, Kirino, Nagaoka, Abe, Nagata and Arai2004) and are not limited to aberrant laryngeal phonation. Motor control is slow and imprecise, thus degrading speech, walking, and other internally guided motor tasks (Harrington & Haaland Reference Harrington and Haaland1991; Marsden & Obeso Reference Marsden and Obeso1994). A suite of cognitive deficits occurs (Flowers & Robertson Reference Flowers and Robertson1985; Lange et al. Reference Lange, Robbins, Marsden, James, Owen and Paul1992), including impairment of cognitive inflexibility and comprehending distinctions in meaning conveyed by syntax (Grossman et al. Reference Grossman, Carvell, Gollomp, Stern, Vernon and Hurtig1991; Lieberman et al. Reference Lieberman, Friedman and Feldman1990; Reference Lieberman, Kako, Friedman, Tajchman, Feldman and Jiminez1992; Natsopoulos et al. Reference Natsopoulos, Grouios, Bostantzopoulou, Mentenopoulos, Katsarou and Logothetis1993). Similar, less pronounced, motor and cognitive deficits occur when hypoxic insult degrades the metabolically active basal ganglia (Lieberman et al. Reference Lieberman, Kanki, Protopapas, Reed and Youngs1994; Reference Lieberman, Morey, Hochstadt, Larson and Mather2005).

These behavioral deficits derive from insult to a network of segregated cortical-to-basal neural circuits linking areas of motor cortex and prefrontal cortex. Marsden and Obeso (Reference Marsden and Obeso1994), taking into account a comprehensive range of studies, concluded that the basal ganglia act as a neural “switch” in circuits linking them to the motor cortex, activating and linking submovements in internally guided acts such as walking or talking. When circumstances suggest a different motor response, the basal ganglia switch to a different sequence. The basal ganglia perform similar operations during cognitive tasks in circuits that include areas of the prefrontal cortex. fMRI studies confirm their supposition. For example, the ventrolateral prefrontal cortex and the caudate nucleus of the basal ganglia are active when a subject is planning to change how he or she is sorting images on the basis of their shapes, to sorting them by color; or selecting words that rhyme and, instead, shifting to selecting words that have similar meanings. A cortical-to-basal ganglia circuit that includes the putamen and posterior prefrontal cortex is active during the execution of a sorting set-shift. The dorsolateral prefrontal cortex is involved whenever subjects make any decision, apparently monitoring whether the subjects' responses were consistent with the chosen sorting criterion (Monchi et al. Reference Monchi, Petrides, Petre, Worsley and Dagher2001; Simard et al. Reference Simard, Joanette, Petrides, Jubault, Madjar and Monchi2011). Other neuroimaging studies, reviewed in Lieberman (Reference Lieberman2000; Reference Lieberman2002; Reference Lieberman2006b; Reference Lieberman2012; Reference Lieberman2013), show that the prefrontal cortex and the basal ganglia are active when subjects have to understand the meaning of a sentence, recall words from memory, subtract numbers, and cognitive tasks. All primates, including humans, appear to have similar cortical-to-basal ganglia circuits (Lehericy et al. Reference Lehericy, Ducros, Van de Moortele, Francois, Thivard, Poupon, Swindale, Ugurbil and Kim2004).

Ackermann et al. instead place great weight on a hypothetical direct cortical-to-laryngeal neural circuit that bypasses the basal ganglia, accepting a premise advanced in Fitch (Reference Fitch2010). The circuit does not exist, being based on flawed attempts to adapt a lethal tracer technique to study humans. The Nauta and Gygax (Reference Nauta and Gygax1954) technique necessitates destroying discrete neural structures in an animal's brain. After some weeks the animal is sacrificed and its brain is impregnated with a silver solution that delineates neuronal structure. Microscopic examination of sectioned brain tissue can then reveal damage to downstream neurons in circuits to the neural structure that was destroyed. Using this technique, Kuypers (Reference Kuypers1958a) and Iwatsubo et al. (Reference Iwatsubo, Kuzuhara, Kanemitsu, Shimada and Toyokura1990) claimed that changes to spinal cord neurons that enervate the larynx revealed a direct cortical-laryngeal circuit. However, the deceased patients studied had massive brain damage that included the basal ganglia and pathways to it. Similar changes to brainstem neurons occurred in patients who had died from non-neurological disease processes (Terao et al. Reference Terao, Li, Hashizume, Osano, Mitsuma and Sobue1997). Jürgens (Reference Jürgens2002b) concludes his review article on the neural bases of motor control by noting that “motor coordination of learned vocal patterns comes from the motor cortex and basal ganglia” (p. 251). Moreover, in itself, enhanced laryngeal control of phonation would not have yielded the encoding of segmental phonemes that is a unique property of human speech (Liberman et al. Reference Liberman, Cooper, Shankweiler and Studdert-Kennedy1967).

Ackermann et al. claim that basal ganglia circuits are devoted to learning “digital” linguistic contrasts in the first years of life, then shift to learning emotional prosody. However, no data are presented to support this claim, and developmental studies show that this is not the case. For example, prosodic patterns signaling intent are apparent in the first year of life in infants in a Catalan-speaking environment (Esteve-Gibert & Prieto Reference Esteve-Gibert and Prieto2013). Both lexical tones and prosodic patterns emerge in the early years of life for Mandarin-learning infants (Chen & Kent Reference Chen and Kent2009).

As my publications have pointed out, transcriptional factors such as FOXP2 may hold the key to why the human brain enables us to talk, continually create new forms of art, and possess language (Lieberman Reference Lieberman2006b; Reference Lieberman2009; Reference Lieberman2013). The basal ganglia, which initially played a role in motor control, appear to have been modified in the course of evolution. The version of FOXP2 that differs with respect to two amino acids from chimpanzees enhances synaptic plasticity in basal ganglia neurons and in the substantia nigra. It also increases dendritic connectivity. A third mutation on FOXP2 (on interon 8, close to the amino acid substitutions) appears to enhance transcription. This uniquely human mutation occurred when modern humans first appeared in Africa (Maricic et al. Reference Maricic, Günther, Georgiev, Gehre, Curlin, Schreiweis, Naumann, Burbano, Meyer, Laluela-Fox, de la Rasilla, Rosas, Gajovic, Kelso, Enard, Schaffner and Pääbo2013). It resulted in a “selective sweep.” Selective sweeps on genetic mutations, such as those that confer adult lactose tolerance (Tishkoff et al. Reference Tishkoff, Reed, Ranciaro, Voight, Babbitt, Silverman, Powell, Mortensen, Hirbo, Osman, Ibrahim, Omar, Lema, Nyambo, Ghori, Bumpstead, Pritchard, Wray and Deloukas2007), occur when a mutation enhances the survival of progeny. One of the tenets of neurophysiology is that synaptic plasticity is the key to learning anything. Virtually all human knowledge is transmitted through the medium of language, and FOXP2 appears to have played a role in the evolution of human language by enhancing basal ganglia synaptic plasticity and connectivity.

It is puzzling that Ackermann et al., disputing my views on the physiology of speech production, included a direct quotation from page 289 of my 2006 book, Toward an Evolutionary Biology of Language. In pages 131 to 245 of this book I discuss, in detail, the issues noted above and other points raised by Ackermann et al.