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Jon Brion was born in Glen Ridge, New Jersey. He came from a musical family: his mother was a jazz singer, his father a band director at Yale, and his brother and sister became a composer/arranger and violinist, respectively. Brion had difficulties in high school and at the age of 17 left education for good, opting instead to play music professionally.

Brion was a member of the band The Bats in the early 1980s, and in 1987 he moved to Boston, where he played solo gigs, formed the short-lived band World's Fair and became a member of the last touring version of Aimee Mann's new wave band 'Til Tuesday. In 1994, joined Dan McCarroll, Buddy Judge and Jellyfish guitarist Jason Falkner in the short-lived pop supergroup The Grays. Brion played numerous instruments on Sam Phillips' 1996 release Omnipop (It's Only A Fleshwound Lambchop).

Brion was signed to the Lava/Atlantic label in 1997, but was released from his contract after turning in his solo debut album Meaningless; the album was released independently in 2001. His own, self-released album Meaningless has won the hearts of his fans, and they eagerly await his 2nd effort.

He has played various instruments on numerous albums, and branched out into production on then-girlfriend Mann's 1993 solo debut, Whatever; he has also produced albums by Fiona Apple, Rufus Wainwright, Eleni Mandell, Rhett Miller and Evan Dando. He is a film composer, garnering Best Score Soundtrack Album Grammy nominations for his work on 1999's Magnolia and 2004's Eternal Sunshine of the Spotless Mind.

In addition to producing, Jon has scored several films, including Magnolia, Punch-Drunk Love, Eternal Sunshine of the Spotless Mind, and I Heart Huckabees. Brion frequently works with director Paul Thomas Anderson, with whom he has a preferential working relationship. In addition to scoring almost all of his films, Brion contributed music to Boogie Nights and had a cameo in the film as a moustachioed guitar player.

Brion is renowned for his regular Friday-night gigs at the Los Angeles club Largo, which feature covers and original songs, a variety of instruments and the quite frequent surprise musical guest. Jon's weekly improvisational cabaret-style act at Largo has reached legend status and is sold out every friday night he performs. But don't be discouraged... if you can bare the wait, you can often get in... and there's usually always room at the 2nd set.

Brion is featured as keyboardist and drummer on Marianne Faithfull's 2003 album, Kissin' Time, and co-wrote a song, "City of Quartz", for her next work, 2005's Before the Poison. Another remarkable work by Brion in the same year was co-producing Kanye West's Late Registration album.

Brion set out on a "tour" of sorts, though in a mid-2005 show he said "don't call it a tour. I'm just going to be moving myself around and playing different cities for weeks at a time". He is also working on his second solo full-length album at Abbey Road Studios.

In April 2006, recurring tendonitis in Brion's right hand forced him to cancel all of his upcoming Largo shows. As a temporary 'farewell', he played his most recent show only using his left hand, even looping his songs as he normally does and playing the drums with one stick.

Recalling his approach to the Largo shows with Chicago Tribune music editor Lou Carlozo, Brion said: "I taught my hands to follow whatever was coming into my head-—and wherever my consciousness would go, I had to push my hands to follow. And at some level, you just had to abandon any concern about how you’d look. Performing without a set list: That was special."

Jon on his Largo performances: "There's no set list. As long as humans keep showing up and paying attention I will keep doing it. I've chosen to do something where both my work and and my life are integrated and both are happening simultaneous every hour I'm awake."