The devil, they say, is in the detail. So too is our fascination with great art. More often than not, the allure of an exceptional work is directly proportional to the controversy generated by an elusive detail crouching ambiguously somewhere within it. To make a list of the most enthralling works in art history is likewise to make a list of those that have provoked the greatest debate about what is actually being depicted. With homage to the author of the celebrated study Seven Types of Ambiguity, the late William Empson (who would have turned 110 last month), what follows are seven of the most contentiously equivocal details in art history.

The Parthenon Marbles (c 447 BC)

Ever since Thomas Bruce, the third Earl of Elgin, shipped from Greece to England in 1802 17 large containers crammed with ancient sculpture pried loose from the Acropolis’s crumbling Athenian Temple, the Parthenon, debate has slowly gathered pace about the rightful ownership of the so-called Elgin Marbles. That controversy, exterior to the work, is mirrored by a quieter aesthetic debate about what, exactly, is being portrayed in a key scene from the 524-ft (159 m) long frieze - a vignette that would have been positioned directly above the entranceway to the temple. Here, a child presents what looks like a folded cloth to an adult. Some interpret the exchange as the bestowal of a ceremonial robe that will be draped over a statue of Athena inside. Others see something rather more gruesome: the daughter of the King of Athens holding her own burial shroud as she is about to be sacrificed as an offering to protect the city-state from invasion.

The Bayeux Tapestry (c 1070s)

Every stitch of the so-called Bayeux Tapestry (it’s actually a 70-metre long embroidered cloth, rather than a woven tapestry) has been pored over by historians desperate to disentangle fact from fiction in its depiction of the events preceding William the Conqueror’s 11th Century invasion of England. Though much has been unravelled regarding its origin (probably the brainchild of William’s half-brother, Bishop Odo) and its creation (likely by a team of gifted seamstresses in the 1070s), several key details continue to needle experts. Chief among these is the strange scene in which a cleric appears to slap (or stroke) a woman’s face, while below them a squatting figure proudly dangles his genitalia.

The Arnolfini Portrait (1434)

Sometimes an orange is just an orange. Occasionally, it must be squeezed into meaning. The latter has certainly been the case with the oranges that loll behind the Italian Merchant Giovanni di Nicolao Arnolfini in a teasing double-portrait by the Early Netherlandish painter Jan Van Eyck, of Arnolfini and his wife - a painting that has puzzled observers since it was created nearly six centuries ago. Every element in the work, from the morphing reflections in the spherical convex mirror at the back of the work to the angle at which the pair’s palms are held, has been prodded for clues about what the work really conveys. Is it, as some contend, a painted pre-nup or a poignant elegy to a deceased wife, as others suggest? Do the oranges (a luxury in the Low Countries in the 15th Century) merely denote impressive financial wealth, or are they a fragrant sign of carnal sin – exotic and fallen?

Madonna and Child with St John (c 1490)

Best known to casual admirers of art history as one of Michelangelo’s first teachers, the Renaissance master Domenico Ghirlandaio has left to posterity a notable visual legacy of his own, including contributions to the decor of the Sistine Chapel, which he undertook a quarter of a century before his legendary pupil would famously tackle the same structure’s ceiling between 1508 and 1512. But it is a curious floating vessel, seen emitting rays of light in the sky behind the Virgin Mary in Ghirlandaio’s Madonna with Saint Giovannino that has attracted the attention of many recent admirers of his work. Does this constitute testimony of a 15th Century extraterrestrial sighting, or is it an awkwardly misshapen angel masquerading as a shiny dirigible?

Mona Lisa (begun 1503)

Is it the mouth or the eyes that truly riddle? Raise the topic of ambiguity in art and the Mona Lisa’s inscrutable expression is invariably submitted as Exhibit A, with attention drawn especially to the indeterminate emotion expressed by her indecipherable lips. Is she smirking at us smugly or barely holding it together by pasting on a polite grin that conceals interior turmoil? Leonardo Da Vinci knew that when the face recites the mute poetry of feeling, the mouth and the eyes invariably rhyme. “It is precisely these parts that Leonardo has left deliberately indistinct”, the celebrated historian EH Gombrich once explained of the artist’s handling of the corners of Mona Lisa’s mouth and eyes, “letting them merge into a soft shadow”. “Her expression always just seems to elude us.”

An Experiment on a Bird in an Air Pump (1768)

Few works of art capture the accelerating fascination with scientific discovery in the 18th Century more dramatically than this one. Created by the English artist and vivid chronicler of the Industrial Revolution, Joseph Wright of Derby, the work teases the observer with the operation of a pneumatic vacuum (following experiments by Robert Boyle a century earlier) in which a cockatoo is slowly being deprived of air - the creature’s very existence hanging in the balance as it levitates in a glass chamber. On the right side of the painting, half-hidden in shadow, a young man holds the rope that lifts and lowers the cage from which the bird has been taken. What is impossible to know, however, is the direction the cage is moving. Is the young man hoisting it because it will no longer be needed, or is he bringing it back down, knowing the bird will survive? The mystery of life and death seems forever to reside in his ambiguous fists.

American Gothic (1930)

Every great work of art has a twist. In the painting that is often described as the most famous work of art in the United States, Grant Wood’s American Gothic (1930) - created the same year that Empson’s Seven Types of Ambiguity was published - the twist takes the form of a serpentine tress that’s fallen loose from the tied-back hair of the prim, apron-clad woman who crowds the double-portrait’s foreground alongside an unflinching farmer. Is the untethered lock proof that the artist is lampooning repressed rural values that are beginning to unravel, or is it a clue to something more symbolically complex? The woman (modelled after Wood’s sister Nan) wears a Persephone brooch, invoking, some believe, the mythological story of that goddess’s rape by Hades. Does Nan’s anxious adjacency to a man brandishing a hayfork (echoing Hades’ signature two-pronged weapon) suggest a modern rehearsal of that brutal myth - her falling hair evidence of a recent ravishing? The devil, they say, is in the detail.

If you would like to comment on this story or anything else you have seen on BBC Culture, head over to our Facebook page or message us on Twitter.

And if you liked this story, sign up for the weekly bbc.com features newsletter, called “If You Only Read 6 Things This Week”. A handpicked selection of stories from BBC Future, Earth, Culture, Capital, Travel and Autos, delivered to your inbox every Friday.